Synaptogenesis in the CNS: An odyssey from wiring together to firing together

Journal of Physiology

Volumn 552, Issue 1, 2003, Pages 1-11

  Munno, David W ^a   Syed, Naweed I ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

SIGNAL PEPTIDE; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCINEURIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM CHANNEL L TYPE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; MEMBRANE ASSOCIATED GUANYLATE CYCLASE KINASE; METHIONINE; MUSCARINIC M1 RECEPTOR; NERVE GROWTH FACTOR; NETRIN; NEUREXIN; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN INTERACTING WITH PROTEIN KINASE C; RAS PROTEIN; ROUNDABOUT RECEPTOR; SLIT PROTEIN; SYNAPTOBREVIN; SYNAPTOBREVIN 2; TRANSCRIPTION FACTOR SOX; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

BRAIN CELL; BRAIN FUNCTION; CELL ADHESION; CELL COMMUNICATION; GROWTH CONE; HUMAN; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVIEW; SYNAPTOGENESIS; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CELL REGENERATION; CELL SELECTION; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; CONNECTOME; EXCITATORY POSTSYNAPTIC POTENTIAL; FIRING RATE; GLUCOSE METABOLISM; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; PRESYNAPTIC MEMBRANE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SYNAPTIC TRANSMISSION;

ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; NEURAL PATHWAYS; NEURONS; SYNAPSES;

EID: 0142030096     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2003.045062     Document Type: Review

References (120)

1. Ahmari SE, Buchanan J & Smith SJ (2000). Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3, 445-451.
2. Ahmari SE & Smith SJ (2002). Knowing a nascent synapse when you see it. Neuron 34, 333-336.
3. Anton ES, Kreidberg JA & Rakic P (1999). Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 22, 277-289.
4. Aravamudan B, Fergestad T, Davis WS, Rodesch CK & Broadie K (1999). Drosophila UNC-13 is essential for synaptic transmission. Nat Neurosci 2, 965-971.
5. Baines RA, Uhler JP, Thompson A, Sweeney ST & Bate M (2001). Altered electrical properties in Drosophila neurons developing without synaptic transmission. J Neurosci 21, 1523-1531.
6. Bennett MK, Calakos N & Scheller RH (1992). Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257, 255-259.
7. Bennett MK, Miller KG & Scheller RH (1993). Casein kinase II phosphorylates the synaptic vesicle protein p65. J Neurosci 13, 1701-1707.
8. Biederer T & Südhof TC (2001). CASK and protein 4.1 support F-actin nucleation on neurexins. J Biol Chem 276, 47869-47876.
9. Braithwaite SP, Xia H & Malenka RC (2002). Differential roles for NSF and GRIP/ABP in AMPA receptor cycling. Proc Natl Acad Sci USA 99, 7096-7101.
10. Brennan C, Rivas-Plata K & Landis SC (1999). The p75 neurotrophin receptor influences NT-3 responsiveness of sympathetic neurons in vivo. Nat Neurosci 2, 699-705.
11. Brenner S (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
12. Brose K & Tessier-Lavigne M (2000). Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr Opin Neurobiol 10, 95-102.
13. Bulloch AG & Syed NI (1992). Reconstruction of neuronal networks in culture. Trends Neurosci 15, 422-427.
14. Butz S, Okamoto M & Sudhof TC (1998). A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell 94, 773-782.
15. Cantallops I & Cline HT (2000). Synapse formation: if it looks like a duck and quacks like a duck. Curr Biol 10, R620-623.
16. Chetkovich DM, Bunn RC, Kuo SH, Kawasaki Y, Kohwi M & Bredt DS (2002a). Postsynaptic targeting of alternative postsynaptic density-95 isoforms by distinct mechanisms. J Neurosci 22, 6415-6425.
17. Chetkovich DM, Chen L, Stocker TJ, Nicoll RA & Bredt DS (2002b). Phosphorylation of the postsynaptic density-95 (PSD-95)/discs large/zona occludens-1 binding site of stargazin regulates binding to PSD-95 and synaptic targeting of AMPA receptors. J Neurosci 22, 5791-5796.
18. Choi-Lundberg DL, Lin Q, Chang YN, Chiang YL, Hay CM, Mohajeri H, Davidson BL & Bohn MC (1997). Dopaminergic neurons protected from degeneration by GDNF gene therapy. Science 275, 838-841.
19. Cohen AR, Woods DF, Marfatia SM, Walther Z, Chishti AH, Anderson JM & Wood DF (1998). Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J Cell Biol 142, 129-138.
20. Einheber S, Schnapp LM, Salzer JL, Cappiello ZB & Milner TA (1996). Regional and ultrastructural distribution of the alpha 8 integrin subunit in developing and adult rat brain suggests a role in synaptic function. J Comp Neurol 370, 105-134.
21. Engert F & Bonhoeffer T (1999). Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70.
22. Erickson JT, Brosenitsch TA & Katz DM (2001). Brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor are required simultaneously for survival of dopaminergic primary sensory neurons in vivo. J Neurosci 21, 581-589.
23. Fagan AM, Zhang H, Landis S, Smeyne RJ, Silos-Santiago I & Barbacid M (1996). TrkA, but not TrkC. receptors are essential for survival of sympathetic neurons in vivo. J Neurosci 16, 6208-6218.
24. 2+ hotspots between Lymnaea neurons during synaptogenesis. J Physiol 539, 53-65.
25. Feng ZP, Klumperman J, Lukowiak K & Syed NI (1997). In vitro synaptogenesis between the somata of identified Lymnaea neurons requires protein synthesis but not extrinsic growth factors or substrate adhesion molecules. J Neurosci 17, 7839-7849.
26. Fernandez de Miguel F & Drapeau P (1995). Synapse formation and function: insights from identified leech neurons in culture. J Neurobiol 27, 367-379.
27. Francis NJ & Landis SC (1999). Cellular and molecular determinants of sympathetic neuron development. Annu Rev Neurosci 22, 541-566.
28. Gao XB & van den Pol AN (2000). GABA release from mouse axonal growth cones. J Physiol 523, 629-637.
29. Giger RJ & Kolodkin AL (2001). Silencing the siren: guidance cue hierarchies at the CNS midline. Cell 105, 1-4.
30. Ginty DD & Segal RA (2002). Retrograde neurotrophin signaling: Trk-ing along the axon. Curr Opin Neurobiol 12, 268-274.
31. Glanzman DL, Kandel ER & Schacher S (1989). Identified target motor neuron regulates neurite outgrowth and synapse formation of Aplysia sensory neurons in vitro. Neuron 3, 441-450.
32. Godenschwege TA, Hu H, Shan-Crofts X, Goodman CS & Murphey RK (2002). Bi-directional signaling by Semaphorin la during central synapse formation in Drosophila. Nat Neurosci 5, 1294-1301.
33. Graus-Porta D, Blaess S, Senften M, Littlewood-Evans A, Damsky C, Huang Z, Orban P, Klein R, Schittny JC & Muller U (2001). Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31, 367-379.
34. Hamakawa T, Woodin MA, Bjorgum MC, Painter SD, Takasaki M, Lukowiak K, Nagle GT & Syed NI (1999). Excitatory synaptogenesis between identified Lymnaea neurons requires extrinsic trophic factors and is mediated by receptor tyrosine kinases. J Neurosci 19, 9306-9312.
35. Hata Y, Butz S & Sudhof TC (1996). 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.
36. Hatten ME (1999). Central nervous system neuronal migration. Annu Rev Neurosci 22, 511-539.
37. Haydon PG (1988). The formation of chemical synapses between cell-cultured neuronal somata. J Neurosci 8, 1032-1038.
38. Haydon PG, Cohan CS, McCobb DP, Miller HR & Kater SB (1985). Neuron-specific growth cone properties as seen in identified neurons of Helisoma. J Neurosci Res 13, 135-147.
39. Haydon PG & Drapeau P (1995). From contact to connection: early events during synaptogenesis. Trends Neurosci 18, 196-201.
40. Haydon PG & Zoran MJ (1989). Formation and modulation of chemical connections: evoked acetylcholine release from growth cones and neurites of specific identified neurons. Neuron 2, 1483-1490.
41. Heerssen HM & Segal RA (2002). Location, location, location: a spatial view of neurotrophin signal transduction. Trends Neurosci 25, 160-165.
42. Ho A, Morishita W, Hammer RE, Malenka RC & Sudhof TC (2003). A role for Mints in transmitter release: Mint 1 knockout mice exhibit impaired GABAergic synaptic transmission. Proc Natl Acad Sci USA 100, 1409-1414.
43. Huang EJ & Reichardt LF (2001). Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24, 677-736.
44. Irie M, Hata Y, Takeuchi M, Ichtchenko K, Toyoda A, Hirao K, Takai Y, Rosahl TW & Sudhof TC (1997). Binding of neuroligins to PSD-95. Science 277, 1511-1515.
45. Jahn R (2000). Sec1/munc18 proteins: mediators of membrane fusion moving to center stage. Neuron 27, 201-204.
46. Kaplan DR & Miller FD (2000). Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10, 381-391.
47. Kim SH, Jen WC, De Robertis EM & Kintner C (2000). The protocadherin PAPC establishes segmental boundaries during somitogenesis in Xenopus embryos. Curr Biol 10, 821-830.
48. Kohara K, Kitamura A, Morishima M & Tsumoto T (2001). Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science 291, 2419-2423.
49. Kolodkin AL (1996). Growth cones and the cues that repel them. Trends Neurosci 19, 507-513.
50. Kopczynski CC, Davis GW & Goodman CS (1996). A neural tetraspanin, encoded by late bloomer, that facilitates synapse formation. Science 271, 1867-1870.
51. Korneev SA, Kemenes I, Straub V, Staras K, Korneeva EI, Kemenes G, Benjamin PR & O'Shea M (2002). Suppression of nitric oxide (NO)-dependent behavior by double-stranded RNA-mediated silencing of a neuronal NO synthase gene. J Neurosci 22, RC227.
52. Lankford KL, Demello FG & Klein WL (1988). D1-type dopamine receptors inhibit growth cone motility in cultured retina neurons: evidence that neurotransmitters act as morphogenic growth regulators in the developing central nervous system. Proc Natl Acad Sci U S A 85, 2839-2843.
53. Lauder JM (1993). Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci 16, 233-240.
54. Lee KJ & Jessell TM (1999). The specification of dorsal cell fates in the vertebrate central nervous system. Annu Rev Neurosci 22, 261-294.
55. Lemke G (2001). Glial control of neuronal development. Annu Rev Neurosci 24, 87-105.
56. Levi-Montalcini R, Skaper SD, Dal Toso R, Petrelli L & Leon A (1996). Nerve growth factor: from neurotrophin to neurokine. Trends Neurosci 19, 514-520.
57. Levitan IB & Kaczmarek LK (2002). The Neuron: Cell and Molecular Biology. Oxford University Press, New York.
58. Liu BP & Strittmatter SM (2001). Semaphorin-mediated axonal guidance via Rho-related G proteins. Curr Opin Cell Biol 13, 619-626.
59. Lovell P, McMahon B & Syed NI (2002). Synaptic precedence during synapse formation between reciprocally connected neurons involves transmitter-receptor interactions and AA metabolites. J Neurophysiol 88, 1328-1338.
60. McAllister AK (2002). Conserved cues for axon and dendrite growth in the developing cortex. Neuron 33, 2-4.
61. McCobb DP, Cohan CS, Connor JA & Kater SB (1988). Interactive effects of serotonin and acetylcholine on neurite elongation. Neuron 1, 377-385.
62. Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH & Kandel ER (1997). Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91, 927-938.
63. Martinez A, Alcantara S, Borrell V, Del Rio JA, Blasi J, Otal R, Campos N, Boronat A, Barbacid M, Silos-Santiago I & Soriano E (1998). TrkB and TrkC signaling are required for maturation and synaptogenesis of hippocampal connections. J Neurosci 18, 7336-7350.
64. Maximov A, Südhof TC & Bezprozvanny I (1999). Association of neuronal calcium channels with modular adaptor proteins. J Biol Chem 274, 24453-24456.
65. Meems R, Munno DW, van Minnen J & Syed NI (2003). Synapse formation between isolated axons requires presynaptic soma and re-distribution of postsynaptic AChRs. J Neurophysiol 89, 2611-2619.
66. Miller FD & Kaplan DR (2001). On Trk for retrograde signaling. Neuron 32, 767-770.
67. Missler M, Fernandez-Chacon R & Südhof TC (1998a). The making of neurexins. J Neurochem 71, 1339-1347.
68. Missler M, Hammer RE & Südhof TC (1998b). Neurexophilin binding to alpha-neurexins. A single LNS domain functions as an independently folding ligand-binding unit. J Biol Chem 273, 34716-34723.
69. Missler M & Südhof TC (1998). Neurexins: three genes and 1001 products. Trends Genet 14, 20-26.
70. Mody M, Cao Y, Cui Z, Tay KY, Shyong A, Shimizu E, Pham K, Schultz P, Welsh D & Tsien JZ (2001). Genome-wide gene expression profiles of the developing mouse hippocampus. Proc Natl Acad Sci U S A 98, 8862-8867.
71. Mueller BK (1999). Growth cone guidance: first steps towards a deeper understanding. Annu Rev Neurosci 22, 351-388.
72. Munno DW, Prince DJ & Syed NI (2003). Synapse number and synaptic efficacy are regulated by presynaptic cAMP and protein kinase A. J Neurosci 23, 4146-4155.
73. Nguyen T & Südhof TC (1997). Binding properties of neuroligin 1 and neurexin 1beta reveal function as heterophilic cell adhesion molecules. J Biol Chem 272, 26032-26039.
74. Nimchinsky EA, Sabatini BL & Svoboda K (2002). Structure and function of dendritic spines. Annu Rev Physiol 64, 313-353.
75. Okabe S, Miwa A & Okado H (2001a). Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J Neurosci 21, 6105-6114.
76. Okabe S, Urushido T, Konno D, Okado H & Sobue K (2001b). Rapid redistribution of the postsynaptic density protein PSD-Zip45 (Homer 1c) and its differential regulation by NMDA receptors and calcium channels. J Neurosci 21, 9561-9571.
77. Okamoto M & Südhof TC (1997). Mints, Munc18-interacting proteins in synaptic vesicle exocytosis. J Biol Chem 272, 31459-31464.
78. Poo MM (2001). Neurotrophins as synaptic modulators. Nat Rev Neurosci 2, 24-32.
79. Rao A, Harms KJ & Craig AM (2000). Neuroligation: building synapses around the neurexin-neuroligin link. Nat Neurosci 3, 747-749.
80. Redies C & Takeichi M (1996). Cadherins in the developing central nervous system: an adhesive code for segmental and functional subdivisions. Dev Biol 180, 413-423.
81. Rice DS & Curran T (2001). Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci 24, 1005-1039.
82. Richmond JE, Weimer RM & Jorgensen EM (2001). An open form of syntaxin bypasses the requirement for UNC-13 in vesicle priming. Nature 412, 338-341.
83. Roos J, Hummel T, Ng N, Klambt C & Davis GW (2000). Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26, 371-382.
84. Sanes JR & Lichtman JW (1999). Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22, 389-442.
85. Sanes JR & Lichtman JW (2001). Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2, 791-805.
86. Schacher S & Wu F (2002). Synapse formation in the absence of cell bodies requires protein synthesis. J Neurosci 22, 1831-1839.
87. Schaefer AM, Hadwiger GD & Nonet ML (2000). rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron 26, 345-356.
88. Schnell E, Sizemore M, Karimzadegan S, Chen L, Bredt DS & Nicoll RA (2002). Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc Natl Acad Sci U S A 99, 13902-13907.
89. Shapiro L & Colman DR (1999). The diversity of cadherins and implications for a synaptic adhesive code in the CNS. Neuron 23, 427-430.
90. Sheng M & Sala C (2001). PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 24, 1-29.
91. 2+ binding site of the synaptotagmin 1 C2B domain triggers fast exocytosis without stimulating SNARE interactions. Neuron 37, 99-108.
92. Smit AB, Syed NI, Schaap D, Van Minnen J, Klumperman J, Kits KS, Lodder H, van der Schors RC, Van Elk R, Sorgedrager B, Brejc K, Sixma TK & Geraerts WP (2001). A glia-derived acetylcholine-binding protein that modulates synaptic transmission. Nature 411, 261-268.
93. Sofroniew MV, Howe CL & Mobley WC (2001). Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 24, 1217-1281.
94. Sollner T, Bennett MK, Whiteheart SW, Scheller RH & Rothman JE (1993a). A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusio. Cell 75, 409-418.
95. Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P & Rothman JE (1993b). SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.
96. Song JY, Ichtchenko K, Südhof TC & Brose N (1999). Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci U S A 96, 1100-1105.
97. Spafford JD, Munno DW, van Nierop P, Feng ZP, Jarvis SE, Gallin WJ, Smit AB, Zamponi GW & Syed NI (2003). Calcium channel structural determinants of synaptic transmission between identified invertebrate neurons. J Biol Chem 278, 4258-4267.
98. Spalding KL, Tan MM, Hendry IA & Harvey AR (2002). Anterograde transport and trophic actions of BDNF and NT-4/5 in the developing rat visual system. Mol Cell Neurosci 19, 485-500.
99. Spencer GE, Klumperman J & Syed NI (1998). Neurotransmitters and neurodevelopment. Role of dopamine in neurite outgrowth, target selection and specific synapse formation. Perspect Dev Neurobiol 5, 451-467.
100. Spencer GE, Lukowiak K & Syed NI (2000). Transmitter-receptor interactions between growth cones of identified Lymnaea neurons determine target cell selection in vitro. J Neurosci 20, 8077-8086.
101. Sperry RW (1963). Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci U S A 50, 703-710.
102. Syed NI, Bulloch AG & Lukowiak K (1990). In vitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science 250, 282-285.
103. Tessier-Lavigne M & Goodman CS (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
104. Tomac A, Lindqvist E, Lin LF, Ogren SO, Young D, Hoffer BJ & Olson L (1995a). Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 373, 335-339.
105. Tomac A, Widenfalk J, Lin LF, Kohno T, Ebendal T, Hoffer BJ & Olson L (1995b). Retrograde axonal transport of glial cell line-derived neurotrophic factor in the adult nigrostriatal system suggests a trophic role in the adult. Proc Natl Acad Sci U S A 92, 8274-8278.
106. van Kesteren RE, Syed NI, Munno DW, Bouwman J, Feng ZP, Geraerts WP & Smit AB (2001). Synapse formation between central neurons requires postsynaptic expression of the MEN1 tumor suppressor gene. J Neurosci 21, RC161.
107. van Vactor D & Flanagan JG (1999). The middle and the end: slit brings guidance and branching together in axon pathway selection. Neuron 22, 649-652.
108. Verhage M, Maia AS, Plomp JJ, Brussaard AB, Heeroma JH, Vermeer H, Toonen RF, Hammer RE, van den Berg TK, Missler M, Geuze HJ & Südhof TC (2000). Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287, 864-869.
109. Wahle P, Di Cristo G, Schwerdtfeger G, Engelhardt M, Berardi N & Maffei L (2003). Differential effects of cortical neurotrophic factors on development of lateral geniculate nucleus and superior colliculus neurons: anterograde and retrograde actions. Development 130, 611-622.
110. Wan HI, Diantonio A, Fetter RD, Bergstrom K, Strauss R & Goodman CS (2000). Highwire regulates synaptic growth in Drosophila. Neuron 26, 313-329.
111. Watson FL, Heerssen HM, Moheban DB, Lin MZ, Sauvageot CM, Bhattacharyya A, Pomeroy SL & Segal RA (1999). Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand-receptor complex. J Neurosci 19, 7889-7900.
112. Woodin MA, Hamakawa T, Takasaki M, Lukowiak K & Syed NI (1999). Trophic factor-induced plasticity of synaptic connections between identified Lymnaea neurons. Learn Mem 6, 307-316.
113. Woodin MA, Munno DW & Syed NI (2002). Trophic factor-induced excitatory synaptogenesis involves postsynaptic modulation of nicotinic acetylcholine receptors. J Neurosci 22, 505-514.
114. Wu MN & Bellen HJ (1997). Genetic dissection of synaptic transmission in Drosophila. Curr Opin Neurobiol 7, 624-630.
115. Wu Q & Maniatis T (1999). A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97, 779-790.
116. Yao WD, Rusch J, Poo M & Wu CF (2000). Spontaneous acetylcholine secretion from developing growth cones of Drosophila central neurons in culture: effects of cAMP-pathway mutations. J Neurosci 20, 2626-2637.
117. Yu HH & Kolodkin AL (1999). Semaphorin signaling: a little less perplexin. Neuron 22, 11-14.
118. Zhen M, Huang X, Bamber B & Jin Y (2000). Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron 26, 331-343.
119. Zheng JQ, Felder M, Connor JA & Poo MM (1994). Turning of nerve growth cones induced by neurotransmitters. Nature 368, 140-144.
120. Zheng JQ, Wan JJ & Poo MM (1996). Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 16, 1140-1149.