Drosophila Neuroligin 1 Promotes Growth and Postsynaptic Differentiation at Glutamatergic Neuromuscular Junctions

Neuron

Volumn 66, Issue 5, 2010, Pages 724-738

  Banovic, Daniel ^a   Khorramshahi, Omid ^b   Owald, David ^b,d   Wichmann, Carolin ^b,c   Riedt, Tamara ^a   Fouquet, Wernher ^b   Tian, Rui ^b   Sigrist, Stephan J ^b   Aberle, Hermann ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c EUROPEAN NEUROSCIENCE INSTITUTE   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Molneuro

Indexed keywords

GLUTAMATE RECEPTOR; NEUREXIN; NEUROLIGIN 1; SCAFFOLD PROTEIN;

ALLELE; ANTIBODY PRODUCTION; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DEVELOPMENT; DROSOPHILA; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; GENETIC SCREENING; IMMUNOHISTOCHEMISTRY; MOLECULAR CLONING; MUTANT; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; SYNAPTIC MEMBRANE; SYNAPTIC TRANSMISSION;

ALLELES; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL DIFFERENTIATION; DROSOPHILA; DROSOPHILA PROTEINS; MUTATION; NEUROMUSCULAR JUNCTION; PRESYNAPTIC TERMINALS; RECEPTORS, GLUTAMATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 77953658943     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.05.020     Document Type: Article

References (62)

1. Aberle H., Haghighi A.P., Fetter R.D., McCabe B.D., Magalhães T.R., Goodman C.S. wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 2002, 33:545-558.
2. Araç D., Boucard A.A., Ozkan E., Strop P., Newell E., Südhof T.C., Brunger A.T. Structures of neuroligin-1 and the neuroligin-1/neurexin-1 beta complex reveal specific protein-protein and protein-Ca2+ interactions. Neuron 2007, 56:992-1003.
3. Atwood H.L., Govind C.K., Wu C.F. Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J. Neurobiol. 1993, 24:1008-1024.
4. Beuchle D., Schwarz H., Langegger M., Koch I., Aberle H. Drosophila MICAL regulates myofilament organization and synaptic structure. Mech. Dev. 2007, 124:390-406.
5. Bischof J., Maeda R.K., Hediger M., Karch F., Basler K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 2007, 104:3312-3317.
6. Biswas S., Russell R.J., Jackson C.J., Vidovic M., Ganeshina O., Oakeshott J.G., Claudianos C. Bridging the synaptic gap: neuroligins and neurexin I in Apis mellifera. PLoS ONE 2008, 3:e3542.
7. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
8. Chih B., Engelman H., Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 2005, 307:1324-1328.
9. Chubykin A.A., Atasoy D., Etherton M.R., Brose N., Kavalali E.T., Gibson J.R., Südhof T.C. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 2007, 54:919-931.
10. Collins C.A., DiAntonio A. Synaptic development: insights from Drosophila. Curr. Opin. Neurobiol. 2007, 17:35-42.
11. Dalva M.B., McClelland A.C., Kayser M.S. Cell adhesion molecules: signalling functions at the synapse. Nat. Rev. Neurosci. 2007, 8:206-220.
12. de Wit J., Sylwestrak E., O'Sullivan M.L., Otto S., Tiglio K., Savas J.N., Yates J.R., Comoletti D., Taylor P., Ghosh A. LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron 2009, 64:799-806.
13. Dean C., Dresbach T. Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci. 2006, 29:21-29.
14. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
15. Dresbach T., Neeb A., Meyer G., Gundelfinger E.D., Brose N. Synaptic targeting of neuroligin is independent of neurexin and SAP90/PSD95 binding. Mol. Cell. Neurosci. 2004, 27:227-235.
16. Drysdale R. FlyBase: a database for the Drosophila research community. Methods Mol. Biol. 2008, 420:45-59. FlyBase Consortium.
17. Fabrichny I.P., Leone P., Sulzenbacher G., Comoletti D., Miller M.T., Taylor P., Bourne Y., Marchot P. Structural analysis of the synaptic protein neuroligin and its beta-neurexin complex: determinants for folding and cell adhesion. Neuron 2007, 56:979-991.
18. Featherstone D.E., Rushton E., Rohrbough J., Liebl F., Karr J., Sheng Q., Rodesch C.K., Broadie K. An essential Drosophila glutamate receptor subunit that functions in both central neuropil and neuromuscular junction. J. Neurosci. 2005, 25:3199-3208.
19. Fouquet W., Owald D., Wichmann C., Mertel S., Depner H., Dyba M., Hallermann S., Kittel R.J., Eimer S., Sigrist S.J. Maturation of active zone assembly by Drosophila Bruchpilot. J. Cell Biol. 2009, 186:129-145.
20. Gilbert M.M., Auld V.J. Evolution of clams (cholinesterase-like adhesion molecules): structure and function during development. Front. Biosci. 2005, 10:2177-2192.
21. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 2004, 119:1013-1026.
22. Grenningloh G., Rehm E.J., Goodman C.S. Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell 1991, 67:45-57.
23. Griffith L.C., Budnik V. Plasticity and second messengers during synapse development. Int. Rev. Neurobiol. 2006, 75:237-265.
24. Hoang B., Chiba A. Single-cell analysis of Drosophila larval neuromuscular synapses. Dev. Biol. 2001, 229:55-70.
25. Hoon M., Bauer G., Fritschy J.M., Moser T., Falkenburger B.H., Varoqueaux F. Neuroligin 2 controls the maturation of GABAergic synapses and information processing in the retina. J. Neurosci. 2009, 29:8039-8050.
26. Ichtchenko K., Hata Y., Nguyen T., Ullrich B., Missler M., Moomaw C., Südhof T.C. Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell 1995, 81:435-443.
27. Ichtchenko K., Nguyen T., Südhof T.C. Structures, alternative splicing, and neurexin binding of multiple neuroligins. J. Biol. Chem. 1996, 271:2676-2682.
28. 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 1997, 277:1511-1515.
29. Jamain S., Quach H., Betancur C., Råstam M., Colineaux C., Gillberg I.C., Soderstrom H., Giros B., Leboyer M., Gillberg C., Bourgeron T. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet. 2003, 34:27-29. Paris Autism Research International Sibpair Study.
30. Jia X.X., Gorczyca M., Budnik V. Ultrastructure of neuromuscular junctions in Drosophila: comparison of wild type and mutants with increased excitability. J. Neurobiol. 1993, 24:1025-1044.
31. Ko J., Fuccillo M.V., Malenka R.C., Südhof T.C. LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron 2009, 64:791-798.
32. Ko J., Zhang C., Arac D., Boucard A.A., Brunger A.T., Südhof T.C. Neuroligin-1 performs neurexin-dependent and neurexin-independent functions in synapse validation. EMBO J. 2009, 28:3244-3255.
33. Koch I., Schwarz H., Beuchle D., Goellner B., Langegger M., Aberle H. Drosophila ankyrin 2 is required for synaptic stability. Neuron 2008, 58:210-222.
34. Laumonnier F., Bonnet-Brilhault F., Gomot M., Blanc R., David A., Moizard M.P., Raynaud M., Ronce N., Lemonnier E., Calvas P., et al. X-linked mental retardation and autism are associated with a mutation in the NLGN4 gene, a member of the neuroligin family. Am. J. Hum. Genet. 2004, 74:552-557.
35. Levinson J.N., Chéry N., Huang K., Wong T.P., Gerrow K., Kang R., Prange O., Wang Y.T., El-Husseini A. Neuroligins mediate excitatory and inhibitory synapse formation: involvement of PSD-95 and neurexin-1beta in neuroligin-induced synaptic specificity. J. Biol. Chem. 2005, 280:17312-17319.
36. Li J., Ashley J., Budnik V., Bhat M.A. Crucial role of Drosophila neurexin in proper active zone apposition to postsynaptic densities, synaptic growth, and synaptic transmission. Neuron 2007, 55:741-755.
37. Lisé M.F., El-Husseini A. The neuroligin and neurexin families: from structure to function at the synapse. Cell. Mol. Life Sci. 2006, 63:1833-1849.
38. Lnenicka G.A., Mellon D. Changes in electrical properties and quantal current during growth of identified muscle fibres in the crayfish. J. Physiol. 1983, 345:261-284.
39. Mahr A., Aberle H. The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr. Patterns 2006, 6:299-309.
40. Missler M., Zhang W., Rohlmann A., Kattenstroth G., Hammer R.E., Gottmann K., Südhof T.C. Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 2003, 423:939-948.
41. Owald D., Fouquet W., Schmidt M., Wichmann C., Mertel S., Depner H., Christiansen F., Zube C., Quentin C., Körner J., et al. A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila. J. Cell Biol. 2010, 188:565-579.
42. Poulopoulos A., Aramuni G., Meyer G., Soykan T., Hoon M., Papadopoulos T., Zhang M., Paarmann I., Fuchs C., Harvey K., et al. Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 2009, 63:628-642.
43. Qin G., Schwarz T., Kittel R.J., Schmid A., Rasse T.M., Kappei D., Ponimaskin E., Heckmann M., Sigrist S.J. Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila. J. Neurosci. 2005, 25:3209-3218.
44. Rasse T.M., Fouquet W., Schmid A., Kittel R.J., Mertel S., Sigrist C.B., Schmidt M., Guzman A., Merino C., Qin G., et al. Glutamate receptor dynamics organizing synapse formation in vivo. Nat. Neurosci. 2005, 8:898-905.
45. Reissner C., Klose M., Fairless R., Missler M. Mutational analysis of the neurexin/neuroligin complex reveals essential and regulatory components. Proc. Natl. Acad. Sci. USA 2008, 105:15124-15129.
46. Sara Y., Biederer T., Atasoy D., Chubykin A., Mozhayeva M.G., Südhof T.C., Kavalali E.T. Selective capability of SynCAM and neuroligin for functional synapse assembly. J. Neurosci. 2005, 25:260-270.
47. Scheiffele P., Fan J., Choih J., Fetter R., Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 2000, 101:657-669.
48. Schmid A., Qin G., Wichmann C., Kittel R.J., Mertel S., Fouquet W., Schmidt M., Heckmann M., Sigrist S.J. Non-NMDA-type glutamate receptors are essential for maturation but not for initial assembly of synapses at Drosophila neuromuscular junctions. J. Neurosci. 2006, 26:11267-11277.
49. Schmid A., Hallermann S., Kittel R.J., Khorramshahi O., Frölich A.M., Quentin C., Rasse T.M., Mertel S., Heckmann M., Sigrist S.J. Activity-dependent site-specific changes of glutamate receptor composition in vivo. Nat. Neurosci. 2008, 11:659-666.
50. Song J.Y., Ichtchenko K., Südhof T.C., Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc. Natl. Acad. Sci. USA 1999, 96:1100-1105.
51. Stapleton M., Liao G., Brokstein P., Hong L., Carninci P., Shiraki T., Hayashizaki Y., Champe M., Pacleb J., Wan K., et al. The Drosophila gene collection: identification of putative full-length cDNAs for 70% of D. melanogaster genes. Genome Res. 2002, 12:1294-1300.
52. Südhof T.C. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 2008, 455:903-911.
53. Takeichi M. The cadherin superfamily in neuronal connections and interactions. Nat. Rev. Neurosci. 2007, 8:11-20.
54. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 1989, 98:81-85.
55. Ushkaryov Y.A., Petrenko A.G., Geppert M., Südhof T.C. Neurexins: synaptic cell surface proteins related to the alpha-latrotoxin receptor and laminin. Science 1992, 257:50-56.
56. Varoqueaux F., Aramuni G., Rawson R.L., Mohrmann R., Missler M., Gottmann K., Zhang W., Südhof T.C., Brose N. Neuroligins determine synapse maturation and function. Neuron 2006, 51:741-754.
57. Wagh D.A., Rasse T.M., Asan E., Hofbauer A., Schwenkert I., Dürrbeck H., Buchner S., Dabauvalle M.C., Schmidt M., Qin G., et al. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 2006, 49:833-844.
58. Washbourne P., Dityatev A., Scheiffele P., Biederer T., Weiner J.A., Christopherson K.S., El-Husseini A. Cell adhesion molecules in synapse formation. J. Neurosci. 2004, 24:9244-9249.
59. Wittenmayer N., Körber C., Liu H., Kremer T., Varoqueaux F., Chapman E.R., Brose N., Kuner T., Dresbach T. Postsynaptic Neuroligin1 regulates presynaptic maturation. Proc. Natl. Acad. Sci. USA 2009, 106:13564-13569.
60. Yamagata M., Sanes J.R., Weiner J.A. Synaptic adhesion molecules. Curr. Opin. Cell Biol. 2003, 15:621-632.
61. Zeng X., Sun M., Liu L., Chen F., Wei L., Xie W. Neurexin-1 is required for synapse formation and larvae associative learning in Drosophila. FEBS Lett. 2007, 581:2509-2516.
62. Zito K., Parnas D., Fetter R.D., Isacoff E.Y., Goodman C.S. Watching a synapse grow: noninvasive confocal imaging of synaptic growth in Drosophila. Neuron 1999, 22:719-729.