How to build a central synapse: Clues from cell culture

Trends in Neurosciences

Volumn 29, Issue 1, 2006, Pages 8-20

  Craig, Ann Marie ^a,b   Graf, Ethan R ^b   Linhoff, Michael W ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CELL PROTEIN; EPHRIN B1; FIBROBLAST GROWTH FACTOR 2; NERVE CELL ADHESION MOLECULE; NEUREXIN; PENTRAXIN; THROMBOSPONDIN 1; THROMBOSPONDIN 2; WNT PROTEIN;

BRAIN DEPTH STIMULATION; CELL ADHESION; CELL CULTURE; CENTRAL NERVOUS SYSTEM; DENDRITIC CELL; GABAERGIC SYSTEM; HUMAN; IN VIVO STUDY; LONGEVITY; NERVE CELL; NERVE CELL PLASTICITY; NERVE CONDUCTION; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; REVIEW; SPINAL CORD NERVE CELL; SYNAPSE; SYNAPTOGENESIS;

ANIMALS; CELLS, CULTURED; GAMMA-AMINOBUTYRIC ACID; GLUTAMATES; HUMANS; MODELS, NEUROLOGICAL; NEURONS; NEUROTRANSMITTER AGENTS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 30344456451     PISSN: 01662236     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tins.2005.11.002     Document Type: Review

References (146)

1. L.C. Katz, and C.J. Shatz Synaptic activity and the construction of cortical circuits Science 274 1996 1133 1138
2. A.M. Craig, and H. Boudin Molecular heterogeneity of central synapses: afferent and target regulation Nat. Neurosci. 4 2001 569 578
3. D.S. Bredt, and R.A. Nicoll AMPA receptor trafficking at excitatory synapses Neuron 40 2003 361 379
4. R. Malinow, and R.C. Malenka AMPA receptor trafficking and synaptic plasticity Annu. Rev. Neurosci. 25 2002 103 126
5. M. Verhage Synaptic assembly of the brain in the absence of neurotransmitter secretion Science 287 2000 864 869
6. F. Varoqueaux Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming Proc. Natl. Acad. Sci. U. S. A. 99 2002 9037 9042
7. K.J. Harms, and A.M. Craig Synapse composition and organization following chronic activity blockade in cultured hippocampal neurons J. Comp. Neurol. 490 2005 72 84
8. C.L. Waites Mechanisms of vertebrate synaptogenesis Annu. Rev. Neurosci. 28 2005 251 274
9. P. Scheiffele Cell-cell signaling during synapse formation in the CNS Annu. Rev. Neurosci. 26 2003 485 508
10. M. Yamagata Synaptic adhesion molecules Curr. Opin. Cell Biol. 15 2003 621 632
11. C. Vicario-Abejon Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons J. Neurosci. 18 1998 7256 7271
12. T.L. Fletcher Synaptogenesis in hippocampal cultures: evidence indicating that axons and dendrites become competent to form synapses at different stages of neuronal development J. Neurosci. 14 1994 6695 6706
13. S. Marty Neurotrophins and activity-dependent plasticity of cortical interneurons Trends Neurosci. 20 1997 198 202
14. L.C. Rutherford Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures J. Neurosci. 17 1997 4527 4535
15. Z.J. Huang BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex Cell 98 1999 739 755
16. X. Jin Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures J. Neurosci. 23 2003 5662 5673
17. O. Krylova WNT-3, expressed by motoneurons, regulates terminal arborization of neurotrophin-3-responsive spinal sensory neurons Neuron 35 2002 1043 1056
18. A.C. Hall Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling Cell 100 2000 525 535
19. Z. Dai, and H.B. Peng Presynaptic differentiation induced in cultured neurons by local application of basic fibroblast growth factor J. Neurosci. 15 1995 5466 5475
20. A.J. Li Fibroblast growth factor-2 increases functional excitatory synapses on hippocampal neurons Eur. J. Neurosci. 16 2002 1313 1324
21. H. Umemori FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain Cell 118 2004 257 270
22. K.S. Christopherson Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis Cell 120 2005 421 433
23. D.H. Mauch CNS synaptogenesis promoted by glia-derived cholesterol Science 294 2001 1354 1357
24. L. Shapiro, and D.R. Colman The diversity of cadherins and implications for a synaptic adhesive code in the CNS Neuron 23 1999 427 430
25. D.L. Benson Molecules, maps and synapse specificity Nat. Rev. Neurosci. 2 2001 899 909
26. C.H. Lee N-cadherin regulates target specificity in the Drosophila visual system Neuron 30 2001 437 450
27. S. Prakash Drosophila N-cadherin mediates an attractive interaction between photoreceptor axons and their targets Nat. Neurosci. 8 2005 443 450
28. K. Irie Roles and modes of action of nectins in cell-cell adhesion Semin. Cell Dev. Biol. 15 2004 643 656
29. T. Biederer SynCAM, a synaptic adhesion molecule that drives synapse assembly Science 297 2002 1525 1531
30. M. Yamagata Sidekicks: synaptic adhesion molecules that promote lamina-specific connectivity in the retina Cell 110 2002 649 660
31. K. Shen, and C.I. Bargmann The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans Cell 112 2003 619 630
32. K. Shen Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1 Cell 116 2004 869 881
33. M.L. Winberg Genetic analysis of the mechanisms controlling target selection: complementary and combinatorial functions of netrins, semaphorins, and IgCAMs Cell 93 1998 581 591
34. M. Missler, and T.C. Sudhof Neurexins: three genes and 1001 products Trends Genet. 14 1998 20 26
35. T. Nguyen, and T.C. Sudhof Binding properties of neuroligin 1 and neurexin 1β reveal function as heterophilic cell adhesion molecules J. Biol. Chem. 272 1997 26032 26039
36. K. Tabuchi, and T.C. Sudhof Structure and evolution of neurexin genes: insight into the mechanism of alternative splicing Genomics 79 2002 849 859
37. A. Stepanyants Class-specific features of neuronal wiring Neuron 43 2004 251 259
38. G.M. Shepherd General and variable features of varicosity spacing along unmyelinated axons in the hippocampus and cerebellum Proc. Natl. Acad. Sci. U. S. A. 99 2002 6340 6345
39. K. Kraszewski Synaptic vesicle dynamics in living cultured hippocampal neurons visualized with CY3-conjugated antibodies directed against the lumenal domain of synaptotagmin J. Neurosci. 15 1995 4328 4342
40. S.R. Krueger The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons Neuron 40 2003 945 957
41. C. Dean Neurexin mediates the assembly of presynaptic terminals Nat. Neurosci. 6 2003 708 716
42. B. Hellwig Synapses on axon collaterals of pyramidal cells are spaced at random intervals: a Golgi study in the mouse cerebral cortex Biol. Cybern. 71 1994 1 12
43. C. Pichitpornchai Morphology of parallel fibres in the cerebellar cortex of the rat: an experimental light and electron microscopic study with biocytin J. Comp. Neurol. 342 1994 206 220
44. A. Peters The Fine Structure of the Nervous System. The Neurons and Supporting cells 1990 Oxford University Press
45. T. Ebihara Synchronized formation and remodeling of postsynaptic densities: long-term visualization of hippocampal neurons expressing postsynaptic density proteins tagged with green fluorescent protein J. Neurosci. 23 2003 2170 2181
46. A.I. Gulyas Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus J. Neurosci. 19 1999 10082 10097
47. M. Megias Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells Neuroscience 102 2001 527 540
48. M. Migliore, and G.M. Shepherd Emerging rules for the distributions of active dendritic conductances Nat. Rev. Neurosci. 3 2002 362 370
49. P. Somogyi Salient features of synaptic organisation in the cerebral cortex Brain Res. Rev. 26 1998 113 135
50. G. Di Cristo Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs Nat. Neurosci. 7 2004 1184 1186
51. F. Ango Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment Cell 119 2004 257 272
52. S. Tuvia The phosphorylation state of the FIGQY tyrosine of neurofascin determines ankyrin-binding activity and patterns of cell segregation Proc. Natl. Acad. Sci. U. S. A. 94 1997 12957 12962
53. A. Nagafuchi, and M. Takeichi Cell binding function of E-cadherin is regulated by the cytoplasmic domain EMBO J. 7 1988 3679 3684
54. Y.S. Chu Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42 J. Cell Biol. 167 2004 1183 1194
55. P. Scheiffele Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons Cell 101 2000 657 669
56. N. Brose Synaptic cell adhesion proteins and synaptogenesis in the mammalian central nervous system Naturwissenschaften 86 1999 516 524
57. Y. Sara Selective capability of SynCAM and neuroligin for functional synapse assembly J. Neurosci. 25 2005 260 270
58. N.E. Ziv, and C.C. Garner Cellular and molecular mechanisms of presynaptic assembly Nat. Rev. Neurosci. 5 2004 385 399
59. O. Prange A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin Proc. Natl. Acad. Sci. U. S. A. 101 2004 13915 13920
60. E.R. Graf Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins Cell 119 2004 1013 1026
61. B. Chih Control of excitatory and inhibitory synapse formation by neuroligins Science 307 2005 1324 1328
62. 2+ channels to synaptic vesicle exocytosis Nature 423 2003 939 948
63. 2+ channels J. Neurosci. 25 2005 4330 4342
64. P.C. Salinas, and S.R. Price Cadherins and catenins in synapse development Curr. Opin. Neurobiol. 15 2005 73 80
65. S.X. Bamji Role of β-catenin in synaptic vesicle localization and presynaptic assembly Neuron 40 2003 719 731
66. C.I. Nam, and L. Chen Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter Proc. Natl. Acad. Sci. U. S. A. 102 2005 6137 6142
67. R.J. O'Brien Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp Neuron 23 1999 309 323
68. R. O'Brien Synaptically targeted NARP plays an essential role in the aggregation of AMPA receptors at excitatory synapses in cultured spinal neurons J. Neurosci. 22 2002 4487 4498
69. R. Mi Differing mechanisms for glutamate receptor aggregation on dendritic spines and shafts in cultured hippocampal neurons J. Neurosci. 22 2002 7606 7616
70. R. Mi AMPA receptor-dependent clustering of synaptic NMDA receptors is mediated by Stargazin and NR2A/B in spinal neurons and hippocampal interneurons Neuron 44 2004 335 349
71. M.B. Dalva EphB receptors interact with NMDA receptors and regulate excitatory synapse formation Cell 103 2000 945 956
72. M.A. Takasu Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors Science 295 2002 491 495
73. R. Klein Eph/ephrin signaling in morphogenesis, neural development and plasticity Curr. Opin. Cell Biol. 16 2004 580 589
74. M. Henkemeyer Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus J. Cell Biol. 163 2003 1313 1326
75. H. Hering, and M. Sheng Dendritic spines: structure, dynamics and regulation Nat. Rev. Neurosci. 2 2001 880 888
76. I.M. Ethell, and E.B. Pasquale Molecular mechanisms of dendritic spine development and remodeling Prog. Neurobiol. 75 2005 161 205
77. P.J. Whiting Molecular and functional diversity of the expanding GABA-A receptor gene family Ann. N. Y. Acad. Sci. 868 1999 645 653
78. J.M. Fritschy, and I. Brunig Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications Pharmacol. Ther. 98 2003 299 323
79. A receptor trafficking, channel activity, and functional plasticity of inhibitory synapses Pharmacol. Ther. 102 2004 195 221
80. F. Fischer Reduced synaptic clustering of GABA and glycine receptors in the retina of the gephyrin null mutant mouse J. Comp. Neurol. 427 2000 634 648
81. S. Levi Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons J. Neurosci. 24 2004 207 217
82. A receptors and gephyrin J. Neurosci. 25 2005 594 603
83. A receptors in mice lacking dystrophin (mdx mice) Eur. J. Neurosci. 11 1999 4457 4462
84. S. Levi Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation J. Neurosci. 22 2002 4274 4285
85. S. Sugita A stoichiometric complex of neurexins and dystroglycan in brain J. Cell Biol. 154 2001 435 445
86. A receptors and gephyrin J. Neurosci. 22 2002 4805 4813
87. J.Y. Song Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses Proc. Natl. Acad. Sci. U. S. A. 96 1999 1100 1105
88. F. Varoqueaux Neuroligin 2 is exclusively localized to inhibitory synapses Eur. J. Cell Biol. 83 2004 449 456
89. D.L. Benson, and H. Tanaka N-cadherin redistribution during synaptogenesis in hippocampal neurons J. Neurosci. 18 1998 6892 6904
90. A. Rao Mismatched appositions of presynaptic and postsynaptic components in isolated hippocampal neurons J. Neurosci. 20 2000 8344 8353
91. J.P. Pierce, and L.M. Mendell Quantitative ultrastructure of Ia boutons in the ventral horn: scaling and positional relationships J. Neurosci. 13 1993 4748 4763
92. K.M. Harris, and J.K. Stevens Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics J. Neurosci. 9 1989 2982 2997
93. T. Schikorski, and C.F. Stevens Quantitative ultrastructural analysis of hippocampal excitatory synapses J. Neurosci. 17 1997 5858 5867
94. H. Taschenberger Optimizing synaptic architecture and efficiency for high-frequency transmission Neuron 36 2002 1127 1143
95. L. Brodin Sequential steps in clathrin-mediated synaptic vesicle endocytosis Curr. Opin. Neurobiol. 10 2000 312 320
96. B. Racz Lateral organization of endocytic machinery in dendritic spines Nat. Neurosci. 7 2004 917 918
97. G. Liu, and R.W. Tsien Properties of synaptic transmission at single hippocampal synaptic boutons Nature 375 1995 404 408
98. B.D. Ackley, and Y. Jin Genetic analysis of synaptic target recognition and assembly Trends Neurosci. 27 2004 540 547
99. K.S. Broadie, and J.E. Richmond Establishing and sculpting the synapse in Drosophila and C. elegans Curr. Opin. Neurobiol. 12 2002 491 498
100. A.W. Dunah LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses Nat. Neurosci. 8 2005 458 467
101. M. Kishi Mammalian SAD kinases are required for neuronal polarization Science 307 2005 929 932
102. D.E. Featherstone Presynaptic glutamic acid decarboxylase is required for induction of the postsynaptic receptor field at a glutamatergic synapse Neuron 27 2000 71 84
103. V.N. Murthy Inactivity produces increases in neurotransmitter release and synapse size Neuron 32 2001 673 682
104. A.E. El-Husseini PSD-95 involvement in maturation of excitatory synapses Science 290 2000 1364 1368
105. N. Uchida The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones J. Cell Biol. 135 1996 767 779
106. A.M. Fannon, and D.R. Colman A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins Neuron 17 1996 423 434
107. J. Spacek, and K.M. Harris Three-dimensional organization of cell adhesion junctions at synapses and dendritic spines in area CA1 of the rat hippocampus J. Comp. Neurol. 393 1998 58 68
108. T.J. Boggon C-cadherin ectodomain structure and implications for cell adhesion mechanisms Science 296 2002 1308 1313
109. W. He Untangling desmosomal knots with electron tomography Science 302 2003 109 113
110. S. Sivasankar Direct measurements of multiple adhesive alignments and unbinding trajectories between cadherin extracellular domains Biophys. J. 80 2001 1758 1768
111. C.R. Monks Three-dimensional segregation of supramolecular activation clusters in T cells Nature 395 1998 82 86
112. M.F. Krummel, and M.M. Davis Dynamics of the immunological synapse: finding, establishing and solidifying a connection Curr. Opin. Immunol. 14 2002 66 74
113. K. Akert Freeze etching and cytochemistry of vesicles and membrane complexes in synapses of the central nervous system G.D. Pappas D.P. Purpura Structure and Function of Synapses 1972 Raven Press 67 86
114. Y. Zuo Development of long-term dendritic spine stability in diverse regions of cerebral cortex Neuron 46 2005 181 189
115. A.J. Holtmaat Transient and persistent dendritic spines in the neocortex in vivo Neuron 45 2005 279 291
116. I.C. Grunwald Hippocampal plasticity requires postsynaptic ephrinBs Nat. Neurosci. 7 2004 33 40
117. O. Bozdagi Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation Neuron 28 2000 245 259
118. G. Liu Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites Nat. Neurosci. 7 2004 373 379
119. C.R. Yu Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map Neuron 42 2004 553 566
120. K.J. Harms Synapse-specific regulation of AMPA receptor subunit composition by activity J. Neurosci. 25 2005 6379 6388
121. J. Burrone Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons Nature 420 2002 414 418
122. A. Prokop Presynaptic development at the Drosophila neuromuscular junction: assembly and localization of presynaptic active zones Neuron 17 1996 617 626
123. W. Lin Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse Nature 410 2001 1057 1064
124. G. Feng Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP Neuron 28 2000 41 51
125. V. De Paola AMPA receptors regulate dynamic equilibrium of presynaptic terminals in mature hippocampal networks Nat. Neurosci. 6 2003 491 500
126. C.S. Chiu Number, density, and surface/cytoplasmic distribution of GABA transporters at presynaptic structures of knock-in mice carrying GABA transporter subtype 1-green fluorescent protein fusions J. Neurosci. 22 2002 10251 10266
127. Y. Sugiyama Determination of absolute protein numbers in single synapses by a GFP-based calibration technique Nat Methods 2 2005 677 684
128. T. Nakagawa Structure and different conformational states of native AMPA receptor complexes Nature 433 2005 545 549
129. J.G. Valtschanoff, and R.J. Weinberg Laminar organization of the NMDA receptor complex within the postsynaptic density J. Neurosci. 21 2001 1211 1217
130. D. Comoletti Characterization of the interaction of a recombinant soluble neuroligin-1 with neurexin-1β J. Biol. Chem. 278 2003 50497 50505
131. J.S. Coggan Evidence for ectopic neurotransmission at a neuronal synapse Science 309 2005 446 451
132. M.B. Kennedy Signal-processing machines at the postsynaptic density Science 290 2000 750 754
133. J.E. Vaughn Fine structure of synaptogenesis in the vertebrate central nervous system Synapse 3 1989 255 285
134. S.E. Ahmari, and S.J. Smith Knowing a nascent synapse when you see it Neuron 34 2002 333 336
135. J.R. Cottrell Distribution, density, and clustering of functional glutamate receptors before and after synaptogenesis in hippocampal neurons J. Neurophysiol. 84 2000 1573 1587
136. Z. Fu Functional excitatory synapses in HEK293 cells expressing neuroligin and glutamate receptors J. Neurophysiol. 90 2003 3950 3957
137. T. Morimoto Calcium-dependent transmitter secretion from fibroblasts: modulation by synaptotagmin I Neuron 15 1995 689 696
138. H. Togashi Cadherin regulates dendritic spine morphogenesis Neuron 35 2002 77 89
139. K. Abe Stability of dendritic spines and synaptic contacts is controlled by α N-catenin Nat. Neurosci. 7 2004 357 363
140. T. Shingai Implications of nectin-like molecule-2/IGSF4/RA175/SgIGSF/ TSLC1/SynCAM1 in cell-cell adhesion and transmembrane protein localization in epithelial cells J. Biol. Chem. 278 2003 35421 35427
141. J.T. Henderson The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function Neuron 32 2001 1041 1056
142. W. Humphrey VMD: visual molecular dynamics J Mol Graph 33-38 1996 27 38
143. G. Rudenko The structure of the ligand-binding domain of neurexin Iβ: regulation of LNS domain function by alternative splicing Cell 99 1999 93 101
144. Y. Bourne Crystal structure of mouse acetylcholinesterase. A peripheral site-occluding loop in a tetrameric assembly J. Biol. Chem. 274 1999 2963 2970
145. J.P. Himanen Crystal structure of an Eph receptor-ephrin complex Nature 414 2001 933 938
146. A.H. Huber Crystal structure of tandem type III fibronectin domains from Drosophila neuroglian at 2.0 Å Neuron 12 1994 717 731