Some assembly required: The development of neuronal synapses

Nature Reviews Molecular Cell Biology

Volumn 4, Issue 11, 2003, Pages 833-841

  Li, Zheng ^a   Sheng, Morgan ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CADHERIN; CELL ADHESION MOLECULE; INTEGRIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUREXIN; PROTEIN TYROSINE KINASE;

BRAIN DEVELOPMENT; CELL COMMUNICATION; CELL MATURATION; DENDRITE; HUMAN; MOLECULAR DYNAMICS; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NERVE FIBER; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SYNAPTOGENESIS;

ANIMALS; AXONS; DENDRITES; HUMANS; SYNAPSES;

EID: 0242551549     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1242     Document Type: Review

References (99)

1. Sanes, J. R. & Lichtman, J. W. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nature Rev. Neurosci. 2, 791-805 (2001)
2. Shatz, C. J. Emergence of order in visual system development. Proc. Natl Acad. Sci. USA 93, 602-608 (1996).
3. Katz, L. C. & Shatz, C. J. Synaptic activity and the constructive of cortical circuits. Science 274, 1133-1138 (1996).
4. Fiala, J. C., Feinberg, M., Popov, V. & Harris, K. M. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci. 18, 8900-8911 (1998). Using serial section EM and three-dimensional analysis, this study showed that numerous asymmetric synapses are formed on dendritic filopodia in the developing rat hippocampus, especially during the first postnatal week.
5. Harris, K. M., Jensen, F. E. & Tsao, B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J. Neurosci. 12, 2685-2705 (1992).
6. Harris, K. M. & Stevens, J. K. Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9, 2982-2997 (1989).
7. Papa, M., Bundman, M. C., Greenberger V. & Segal, M Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. J. Neurosci. 15, 1-11 (1995).
8. Boyer, C., Schikorski, T. & Stevens, C. F. Comparison of hippocampal dendritic spines in culture and in brain. J. Neurosci. 18, 5294-5300 (1998).
9. Hering, H. & Sheng, M. Dendritic spines: structure, dynamics and regulation. Nature Rev. Neurosci. 2, 880-880 (2001).
10. Harris, K. M. & Kater, S. B. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu. Rev. Neurosci. 17, 341-371 (1994).
11. Miller, M. & Peters, A. Maturation of rat visual cortex. II. A combined Golgi-electron microscope study of pyramidal neurons. J. Comp. Neurol. 203, 555-573 (1981).
12. Harris, K. M. Structure, development, and plasticity of dendritic spines. Curr. Opin. Neurobiol. 9, 343-348 (1999).
13. Dailey, M. E. & Smith, S. J. The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16, 2983-2994 (1996).
14. Ziv, N. E. & Smith, S. J. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17 91-102 (1996).
15. Saito, Y. et al. Developing corticorubral axons of the cat form synapses on filopodial dendritic protrusions. Neurosci. Lett. 147, 81-84 (1992).
16. Ahmari, S. E., Buchanan, J. & Smith, S. J. Assembly of presynaptic active zones from cytoplasmic transport packets. Nature Neurosci. 3, 445-451 (2000). Based on time-lapse fluorescence imaging, immunocytochemistry and EM, this study indicates that the presynaptic specialization is rapidly assembled from prefabricated packets, and that these packets contain active-zone proteins and synaptic-vesicle proteins that are associated with vesicular and tubulovesicular membrane structures.
17. Friedman, H. V., Bresler T., Garner C. C. & Ziv, N. E. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27, 57-69 (2000). The temporal order of presynaptic and postsynaptic protein accumulation after axon-dendrite contact was determined using time-lapse microscopy and retrospective immunohistochemistry. The study indicates that presynaptic differentiation precedes postsynaptic differentiation.
18. Okabe, S., Miwa, A. & Okado, H. Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J. Neurosci. 21, 6105-6114 (2001). The temporal sequence of the accumulation of presynaptic (synaptophysin) and postsynaptic (PSD-95) proteins at synapses was examined using dual-wavelength time-lapse imaging, and was correlated with dendritic-spine morphogenesis in cultured hippocampal neurons.
19. Yagi, T. & Takeichi, M. Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev. 14, 1169-1180 (2000)
20. Togashi, H. et al. Cadherin regulates dendritic spine morphogenesis. Neuron 35, 77-89 (2002).
21. Pinkstaff, J. K., Detterich, J., Lynch, G. & Gall, C. Integrin subunit gene expression is regionally differentiated in adult brain. J. Neurosci. 19, 1541-1556 (1999).
22. Aplin, A. E., Howe, A., Alahari, S. K. & Juliano, R. L. Signal transduction and signal modulation by cell adhesion receptors: the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins. Pharmacol. Rev. 50, 197-263 (1998).
23. Milner, R. & Campbell, L. The integrin family of cell adhesion molecules has multiple functions within the CNS. J. Neurosci. Res. 69, 286-291 (2002).
24. Pasterkamp, R. J., Peschon, J. J., Spriggs, M. K. & Kolodkin, A. L. Semaphorin 7A promotes axon outgrowth through integrins and MAPKs. Nature 424, 398-405 (2003).
25. Hoang, B. & Chiba, A. Genetic analysis on the role of integrin during axon guidance in Drosophila. J. Neurosci. 18, 7847-7855 (1998).
26. Chavis, P. & Westbrook, G. Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse Nature 411, 317-321 (2001).
27. Chan, C. S., Weeber, E. J., Kurup, S., Sweatt, J. D. & Davis, R. L. Integrin requirement for hippocampal synaptic plasticity and spatial memory. J. Neurosci. 23, 7107-7116 (2003).
28. Missler, M., Fernandez-Chacon, R. & Sudhof, T. C. The making of neurexins. J. Neurochem. 71, 1339-1347 (1998).
29. Scheiffele, P., Fan, J., Choih, J., Fetter R. & Serafini, T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101, 657-669 (2000).
30. Irie, M. et al. Binding of nouroligins to PSD-95. Science 277, 1511-1515 (1997).
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, 2488-2494 (1996).
32. 2--channels to synaptic vesicle exocytosis. Nature 424, 939-948 (2003).
33. Biederer, T. et al. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297, 1525-1531 (2002). A new immunoglobulin-domain-containing protein - SynCAM - is cloned, which is present at synapses and promotes synapse formation in vitro.
34. Ethell, I. M. et al. EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron 31, 1001-1013 (2001).
35. Penzes, P. et al. Rapid induction of dendritic spine morphogenesis by trans-synaptic eprinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37, 263-274 (2003). The ephrinB-EphB-receptor trans-synaptic signalling pathway was found to regulate the morphogenesis of dendritic spines through the activation of Rac1 in hippocampal neurons.
36. Takasu, M. A., Dalva, M. B., Zigmond, R. E. & Greenberg, M. E. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295, 491-495 (2002).
37. Dalva, M. B. et al. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103, 945-956 (2000).
38. Henderson, J. T. et al. The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron 32, 1041-1056 (2001).
39. Grunwald, I. C. et al. Kinase-independent requirement of EphB2 receptors in hippocampal synaptic plasticity. Neuron 32, 1027-1040 (2001).
40. Washbourne, P., Bennett, J. E. & McAllister, A. K. Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nature Neurosci. 5, 751-759 (2002). The movement of NMDA- and AMPA-receptor clusters and their time course of recruitment to nascent synapses was determined using time-lapse imaging of cultured cortical neurons.
41. 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, 1217-1229 (1998).
42. Sans, N. et al. A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J. Neurosci. 20, 1260-1271 (2000).
43. Schikorski, T. & Stevens, C. F. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 17, 5858-5867 (1997).
44. Zhai, R. G. et al. Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 29, 131-143 (2001). This paper identified a dense-core-vesicle population that contains presynaptic active-zone proteins and probably functions as a transport packet for the assembly of the presynaptic active zone.
45. Shapira, M. et al. Unitary assembly of presynaptic active zones from piccolo-bassoon transport vesicles. Neuron 38, 237-252 (2003).
46. Zhal, R. et al. Temporal appearance of the presynaptic cytomatrix protein bassoon during synaptogenesis. Mol. Cell. Neurosci. 15, 417-428 (2000).
47. Marrs. G. S., Green, S. H. & Dailey, M. E. Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nature Neurosci. 4, 1006-1013 (2001).
48. El-Husseini, A. E. et al. Dual palmitoylation of PSD-95 mediates its vesiculotubular sorting, postsynaptic targeting, and ion channel clustering. J. Cell Biol. 148, 159-172 (2000).
49. Bresler, T. et al. The dynamics of SAP90/PSD-95 recruitment to new synaptic junctions. Mol. Cell. Neurosci. 18, 149-167 (2001).
50. Migaud, M. et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396, 433-439 (1998).
51. Passafaro, M., Sala, C., Niethammer M. & Sheng, M. Microtubule binding by CRIPT and its potential role in the synaptic clustering of PSD-95. Nature Neurosci. 2, 1063-1069 (1999).
52. Sprengel, R. et al. Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell 92, 279-289 (1998).
53. Scannevin, R. H. & Huganir R. L. Postsynaptic organization and regulation of excitatory synapses. Nature Rev. Neurosci. 1, 133-141 (2000).
54. Sheng, M. & Sala, C. PDZ domains and the organization of supramolecular complexes. Annu. Rev. Neurosci. 24, 1-29 (2001). This review summarizes the structure and function of PDZ domains and the cell-biological roles of PDZ-domain-containing scaffold proteins.
55. Sheng, M. & Pak, D. T. Ligand-gated ion channel interactions with cytoskeletal and signaling proteins. Annu. Rev. Physiol. 62, 755-778 (2000).
56. Barry, M. F. & Ziff, E. B. Receptor trafficking and the plasticity of excitatory synapses. Curr. Opin. Neurobiol. 12, 279-286 (2002).
57. Chen, L. et al. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408, 936-943 (2000).
58. Blue, M. E. & Parnavelas, J. G. The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. J. Neurocytol. 12, 697-712 (1983).
59. Liao, D., Hessler, N. A. & Malinow, R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400-404 (1995).
60. Isaac, J. T., Crair M. C., Nicoll, R. A. & Malenka, R. C. Silent synapses during development of thalamocortical inputs. Neuron 18, 269-280 (1997).
61. Durand, G. M., Kovalchuk, Y. & Konnerth, A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381, 71-75 (1996).
62. Wu, G., Malinow, R. & Cline, H. T. Maturation of a central glutamatergic synapse. Science 274, 972-976 (1996)
63. Nusser, Z. et al. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21, 545-559 (1998).
64. Liao, D., Zhang, X., O'Brien, R., Ehlers, M. D. & Huganir, R. L. Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nature Neurosci. 2, 37-43 (1999).
65. Gomperts, S. N., Rao, A., Craig, A. M., Malenka, R. C. & Nicoll, R. A. Postsynaptically silent synapses in single neuron cultures. Neuron 21, 1443-1451 (1998).
66. Petralia, R. S. et al. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nature Neurosci. 2, 31-36 (1999).
67. Matsuzaki, M. et al. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nature 4, 1086-1092 (2001). Using two-photon excitation of caged-glutamate and electrophysiology studies, the distribution and density of functional AMPA receptors was shown to correlate with the spine-head volume.
68. Zhu, J. J. & Malinow, R. Acute versus chronic NMDA receptor blockade and synaptic AMPA receptor delivery. Nature Neurosci. 5, 513-514 (2002).
69. Zhu, J. J., Esteban, J. A., Hayashi, Y. & Malinow, R. Postnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity. Nature Neurosci. 3, 1096-1106 (2000). This study showed that GluR4-containing AMPA receptors are recruited to synapses in response to spontaneous synaptic activity that required the activation of NMDA receptors, but not CaMKII.
70. Passafaro, M., Nakagawa, T., Sala, C. & Sheng, M. Induction of dendritic spines by an extracellular domain of AMPA receptor subunit GluR2. Nature 424, 677-681 (2003). The extracellular amino-terminal domain of AMPA-receptor-subunit GluR2 is shown to be important for promoting dendritic-spine formation and growth.
71. Bozdagi, O., Shan, W., Tanaka, H., Benson, D. L. & Huntley, G. W. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28, 245-259 (2000).
72. Murase, S., Mosser, E. & Schuman, E. M. Depolarization drives β-catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35, 91-105 (2002).
73. Liu, G. Presynaptic control of quantal size: kinetic mechanisms and implications for synaptic transmission and plasticity. Curr. Opin. Neurobiol. 13, 324-331 (2003).
74. Renger, J. J., Egles, C. & Liu, G. A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation. Neuron 29, 469-484 (2001).
75. Patneau, D. K. & Mayer, M. L. Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J. Neurosci. 10, 2385-2399 (1990).
76. Wu, G. Y. & Cline, H. T. Stabilization of dendritic arbor structure in vivo by CaMKII. Science 279, 222-226 (1998).
77. Zou, D. J. & Cline, H. T. Postsynaptic calcium/calmodulin-dependent protein kinase II is required to limit elaboration of presynaptic and postsynaptic neuronal arbors. J. Neurosci. 19, 8909-8918 (1999).
78. Ben-Ari, Y. Excitatory actions of gaba during development: the nature of the nurture. Nature Rev. Neurosci. 3, 728-739 (2002).
79. Ganguly, K., Schinder, A. F., Wong, S. T. & Poo, M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105, 521-532 (2001).
80. - cotransport distinguishes depolarizing from hyperpolarizing GABAA receptor-mediated responses in spinal neurons. J. Neurosci. 16, 82-91 (1996).
81. Rivera, C. et al. The K-/Cl-co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397, 251-255 (1999).
82. 2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus. Neuron 18, 243-255 (1997).
83. Tyzio, R. et al. 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, 10372-10382 (1999).
84. Khazipov, R. et al. Early development of neuronal activity in the primate hippocampus in utero. J. Neurosci. 21, 9770-9781 (2001).
85. Cohen-Cory S. The developing synapse: construction and modulation of synaptic structures and circuits. Science 298, 770-776 (2002).
86. Augustin, I., Rosenmund, C., Sudhof, T. C. & Brose, N. Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400, 457-461 (1999).
87. Varoqueaux, F. et al. Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc. Natl Acad. Sci. USA 99, 9037-9042 (2002).
88. Verhage, M. et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287, 864-869 (2000). In references 87 and 88, morphologically normal synapses are observed in the brains of mice that are deficient for synaptic transmission.
89. O'Brien, R. et al. Synaptically targeted narp plays an essential role in the aggregation of AMPA receptors at excitatory synapses in cultured spinal neurons. J. Neurosci. 22, 4487-4498 (2002).
90. O'Brien, R. J. et al. Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 23, 309-323 (1999).
91. Abede, H. et al. wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33, 545-558 (2002).
92. Marques, G. et al. The Drosophila BMP type II receptor Wishful Thinking regulates neuromuscular synapse morphology and function. Neuron 33, 529-543 (2002).
93. Packard, M. et al. The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell 11, 319-330 (2002).
94. Hall, A. C., Lucas, F. R. & Salinas, P. C. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100, 525-535 (2000).
95. Ullian, E. M., Sapperstein, S. K., Christopherson, K. S. & Barres, B. A. Control of synapse number by glia. Science 291, 657-661 (2001). This study shows that, in the absence of glia, cultured neurons form sparse and functionally immature synapses. Glia are therefore crucial for synaptogenesis and synapse maturation.
96. Pfrieger, F. W. & Barres, B. A. Synaptic efficacy enhanced by glial cells in vitro. Science 277, 1684-1687 (1997).
97. Mauch, D. H. et al. CNS synaptogenesis promoted by glia-derived cholesterol. Science 294, 1354-1357 (2001).
98. Hering, H., Lin, C. C. & Sheng, M. Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci. 23, 3262-3271 (2003).
99. Beattie, E. C. et al. Control of synaptic strength by glial TNFα. Science 295, 2282-2285 (2002).