Crucial Role of Drosophila Neurexin in Proper Active Zone Apposition to Postsynaptic Densities, Synaptic Growth, and Synaptic Transmission

Neuron

Volumn 55, Issue 5, 2007, Pages 741-755

  Li, Jingjun ^a   Ashley, James ^b   Budnik, Vivian ^b   Bhat, Manzoor A ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

CELLBIO; DEVBIO; MOLNEURO

Indexed keywords

NEUREXIN;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; DROSOPHILA; FEMALE; MALE; MUTATION; NERVE CELL; NEUROMUSCULAR SYNAPSE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; CELL ADHESION; CELL ADHESION MOLECULES, NEURONAL; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MOLECULAR SEQUENCE DATA; MOTOR NEURONS; MUTATION; NEUROMUSCULAR JUNCTION; PRESYNAPTIC TERMINALS; SEQUENCE HOMOLOGY, AMINO ACID; SYNAPSES; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION;

EID: 34548316270     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.08.002     Document Type: Article

References (78)

1. Adams M.D., Celniker S.E., Holt R.A., Evans C.A., Gocayne J.D., Amanatides P.G., Scherer S.E., Li P.W., Hoskins R.A., Galle R.F., et al. The genome sequence of Drosophila melanogaster. Science 287 (2000) 2185-2195
2. Adams M.D., McVey M., and Sekelsky J.J. Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science 299 (2003) 265-267
3. Ashley J., Packard M., Ataman B., and Budnik V. Fasciclin II signals new synapse formation through amyloid precursor protein and the scaffolding protein dX11/Mint. J. Neurosci. 25 (2005) 5943-5955
4. Atasoy D., Schoch S., Ho A., Nadasy K.A., Liu X., Zhang W., Mukherjee K., Nosyreva E.D., Fernandez-Chacon R., Missler M., et al. Deletion of CASK in mice is lethal and impairs synaptic function. Proc. Natl. Acad. Sci. USA 104 (2007) 2525-2530
5. Banerjee S., Pillai A.M., Paik R., Li J., and Bhat M.A. Axonal ensheathment and septate junction formation in the peripheral nervous system of Drosophila. J. Neurosci. 26 (2006) 3319-3329
6. Baumgartner S., Littleton J.T., Broadie K., Bhat M.A., Harbecke R., Lengyel J.A., Chiquet-Ehrismann R., Prokop A., and Bellen H.J. A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87 (1996) 1059-1068
7. Bellen H.J., and Budnik V. The neuromuscular junction. In: Ashburner M., Hawley S., and Sullivan B. (Eds). Drosophila, A Laboratory Manual (2000), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 175-199
8. Bellen H.J., Lu Y., Beckstead R., and Bhat M.A. Neurexin IV, caspr and paranodin-novel members of the neurexin family: encounters of axons and glia. Trends Neurosci. 21 (1998) 444-449
9. Bhat M.A., Rios J.C., Lu Y., Garcia-Fresco G.P., Ching W., St Martin M., Li J., Einheber S., Chesler M., Rosenbluth J., et al. Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 30 (2001) 369-383
10. Biederer T., and Sudhof T.C. Mints as adaptors. Direct binding to neurexins and recruitment of munc18. J. Biol. Chem. 275 (2000) 39803-39806
11. Boucard A.A., Chubykin A.A., Comoletti D., Taylor P., and Sudhof T.C. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron 48 (2005) 229-236
12. Budnik V., Koh Y.H., Guan B., Hartmann B., Hough C., Woods D., and Gorczyca M. Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron 17 (1996) 627-640
13. Chih B., Engelman H., and Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 307 (2005) 1324-1328
14. Chih B., Gollan L., and Scheiffele P. Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51 (2006) 171-178
15. Comoletti D., Flynn R.E., Boucard A.A., Demeler B., Schirf V., Shi J., Jennings L.L., Newlin H.R., Sudhof T.C., and Taylor P. Gene selection, alternative splicing, and post-translational processing regulate neuroligin selectivity for beta-neurexins. Biochemistry 45 (2006) 12816-12827
16. Connolly J.B., and Tully T. Behaviour, learning, and memory. In: Roberts D.B. (Ed). Drosophila, A Practical Approach (1998), Oxford University Press, New York 265-317
17. Coyle I.P., Koh Y.H., Lee W.C., Slind J., Fergestad T., Littleton J.T., and Ganetzky B. Nervous wreck, an SH3 adaptor protein that interacts with Wsp, regulates synaptic growth in Drosophila. Neuron 41 (2004) 521-534
18. Dean C., Scholl F.G., Choih J., DeMaria S., Berger J., Isacoff E., and Scheiffele P. Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 6 (2003) 708-716
19. Deng W.M., Schneider M., Frock R., Castillejo-Lopez C., Gaman E.A., Baumgartner S., and Ruohola-Baker H. Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila. Development 130 (2003) 173-184
20. Faivre-Sarrailh C., Banerjee S., Li J., Hortsch M., Laval M., and Bhat M.A. Drosophila contactin, a homolog of vertebrate contactin, is required for septate junction organization and paracellular barrier function. Development 131 (2004) 4931-4942
21. Fu Z., Washbourne P., Ortinski P., and Vicini S. Functional excitatory synapses in HEK293 cells expressing neuroligin and glutamate receptors. J. Neurophysiol. 90 (2003) 3950-3957
22. Geppert M., Goda Y., Hammer R.E., Li C., Rosahl T.W., Stevens C.F., and Sudhof T.C. Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79 (1994) 717-727
23. Gerrow K., and El-Husseini A. Cell adhesion molecules at the synapse. Front. Biosci. 11 (2006) 2400-2419
24. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., and Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119 (2004) 1013-1026
25. Graf E.R., Kang Y., Hauner A.M., and Craig A.M. Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 beta LNS domain. J. Neurosci. 26 (2006) 4256-4265
26. Griffith L.C., and Budnik V. Plasticity and second messengers during synapse development. Int. Rev. Neurobiol. 75 (2006) 237-265
27. Harden N., Lee J., Loh H.Y., Ong Y.M., Tan I., Leung T., Manser E., and Lim L. A Drosophila homolog of the Rac- and Cdc42-activated serine/threonine kinase PAK is a potential focal adhesion and focal complex protein that colocalizes with dynamic actin structures. Mol. Cell. Biol. 16 (1996) 1896-1908
28. Hata Y., Davletov B., Petrenko A.G., Jahn R., and Sudhof T.C. Interaction of synaptotagmin with the cytoplasmic domains of neurexins. Neuron 10 (1993) 307-315
29. Hata Y., Butz S., and 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 (1996) 2488-2494
30. Ho A., Morishita W., Hammer R.E., Malenka R.C., and Sudhof T.C. A role for Mints in transmitter release: Mint 1 knockout mice exhibit impaired GABAergic synaptic transmission. Proc. Natl. Acad. Sci. USA 100 (2003) 1409-1414
31. Hummel T., Krukkert K., Roos J., Davis G., and Klambt C. Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26 (2000) 357-370
32. Ichtchenko K., Hata Y., Nguyen T., Ullrich B., Missler M., Moomaw C., and Sudhof T.C. Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell 81 (1995) 435-443
33. Irie M., Hata Y., Takeuchi M., Ichtchenko K., Toyoda A., Hirao K., Takai Y., Rosahl T.W., and Sudhof T.C. Binding of neuroligins to PSD-95. Science 277 (1997) 1511-1515
34. Kattenstroth G., Tantalaki E., Sudhof T.C., Gottmann K., and Missler M. Postsynaptic N-methyl-D-aspartate receptor function requires alpha-neurexins. Proc. Natl. Acad. Sci. USA 101 (2004) 2607-2612
35. Kawasaki F., Zou B., Xu X., and Ordway R.W. Active zone localization of presynaptic calcium channels encoded by the cacophony locus of Drosophila. J. Neurosci. 24 (2004) 282-285
36. Kittel R.J., Wichmann C., Rasse T.M., Fouquet W., Schmidt M., Schmid A., Wagh D.A., Pawlu C., Kellner R.R., Willig K.I., et al. Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 312 (2006) 1051-1054
37. Koh T.W., Verstreken P., and Bellen H.J. Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43 (2004) 193-205
38. Kumar S., Tamura K., and Nei M. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief. Bioinform. 5 (2004) 150-163
39. Lahey T., Gorczyca M., Jia X.X., and Budnik V. The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 13 (1994) 823-835
40. Levinson J.N., Chery N., Huang K., Wong T.P., Gerrow K., Kang R., Prange O., Wang Y.T., and 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. 280 (2005) 17312-17319
41. Lin D.M., and Goodman C.S. Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 13 (1994) 507-523
42. Littleton J.T., and Ganetzky B. Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26 (2000) 35-43
43. Littleton J.T., Bellen H.J., and Perin M.S. Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse. Development 118 (1993) 1077-1088
44. Marie B., Sweeney S.T., Poskanzer K.E., Roos J., Kelly R.B., and Davis G.W. Dap160/intersectin scaffolds the periactive zone to achieve high-fidelity endocytosis and normal synaptic growth. Neuron 43 (2004) 207-219
45. Marrus S.B., Portman S.L., Allen M.J., Moffat K.G., and DiAntonio A. Differential localization of glutamate receptor subunits at the Drosophila neuromuscular junction. J. Neurosci. 24 (2004) 1406-1415
46. McVey M., Larocque J.R., Adams M.D., and Sekelsky J.J. Formation of deletions during double-strand break repair in Drosophila DmBlm mutants occurs after strand invasion. Proc. Natl. Acad. Sci. USA 101 (2004) 15694-15699
47. Meyer G., Varoqueaux F., Neeb A., Oschlies M., and Brose N. The complexity of PDZ domain-mediated interactions at glutamatergic synapses: a case study on neuroligin. Neuropharmacology 47 (2004) 724-733
48. Missler M., and Sudhof T.C. Neurexins: three genes and 1001 products. Trends Genet. 14 (1998) 20-26
49. Missler M., Zhang W., Rohlmann A., Kattenstroth G., Hammer R.E., Gottmann K., and Sudhof T.C. Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 423 (2003) 939-948
50. Murthy V.N., Schikorski T., Stevens C.F., and Zhu Y. Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32 (2001) 673-682
51. Nam C.I., and Chen L. Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc. Natl. Acad. Sci. USA 102 (2005) 6137-6142
52. O'Brien R.J., Kamboj S., Ehlers M.D., Rosen K.R., Fischbach G.D., and Huganir R.L. Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 21 (1998) 1067-1078
53. Peles E., Joho K., Plowman G.D., and Schlessinger J. Close similarity between Drosophila neurexin IV and mammalian Caspr protein suggests a conserved mechanism for cellular interactions. Cell 88 (1997) 745-746
54. Petersen S.A., Fetter R.D., Noordermeer J.N., Goodman C.S., and DiAntonio A. Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 19 (1997) 1237-1248
55. Poliak S., Gollan L., Martinez R., Custer A., Einheber S., Salzer J.L., Trimmer J.S., Shrager P., and Peles E. Caspr2, a new member of the neurexin superfamily, is localized at the juxtaparanodes of myelinated axons and associates with K+ channels. Neuron 24 (1999) 1037-1047
56. Prange O., Wong T.P., Gerrow K., Wang Y.T., and El-Husseini A. A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin. Proc. Natl. Acad. Sci. USA 101 (2004) 13915-13920
57. Prokop A., and Meinertzhagen I.A. Development and structure of synaptic contacts in Drosophila. Semin. Cell Dev. Biol. 17 (2006) 20-30
58. Roos J., and Kelly R.B. The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr. Biol. 9 (1999) 1411-1414
59. Roos J., Hummel T., Ng N., Klambt C., and Davis G.W. Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26 (2000) 371-382
60. Rowen L., Young J., Birditt B., Kaur A., Madan A., Philipps D.L., Qin S., Minx P., Wilson R.K., Hood L., and Graveley B.R. Analysis of the human neurexin genes: alternative splicing and the generation of protein diversity. Genomics 79 (2002) 587-597
61. Scheiffele P. Cell-cell signaling during synapse formation in the CNS. Annu. Rev. Neurosci. 26 (2003) 485-508
62. Scheiffele P., Fan J., Choih J., Fetter R., and Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101 (2000) 657-669
63. Shcherbata H.R., Yatsenko A.S., Patterson L., Sood V.D., Nudel U., Yaffe D., Baker D., and Ruohola-Baker H. Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. EMBO J. 26 (2007) 481-493
64. Smith L.A., Wang X., Peixoto A.A., Neumann E.K., Hall L.M., and Hall J.C. A Drosophila calcium channel alpha1 subunit gene maps to a genetic locus associated with behavioral and visual defects. J. Neurosci. 16 (1996) 7868-7879
65. Sone M., Suzuki E., Hoshino M., Hou D., Kuromi H., Fukata M., Kuroda S., Kaibuchi K., Nabeshima Y., and Hama C. Synaptic development is controlled in the periactive zones of Drosophila synapses. Development 127 (2000) 4157-4168
66. Song J.Y., Ichtchenko K., Sudhof T.C., and Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc. Natl. Acad. Sci. USA 96 (1999) 1100-1105
67. Stewart B.A., Schuster C.M., Goodman C.S., and Atwood H.L. Homeostasis of synaptic transmission in Drosophila with genetically altered nerve terminal morphology. J. Neurosci. 16 (1996) 3877-3886
68. Sugita S., Saito F., Tang J., Satz J., Campbell K., and Sudhof T.C. A stoichiometric complex of neurexins and dystroglycan in brain. J. Cell Biol. 154 (2001) 435-445
69. Tabuchi K., and Sudhof T.C. Structure and evolution of neurexin genes: insight into the mechanism of alternative splicing. Genomics 79 (2002) 849-859
70. Taniguchi H., Gollan L., Scholl F.G., Mahadomrongkul V., Dobler E., Limthong N., Peck M., Aoki C., and Scheiffele P. Silencing of neuroligin function by postsynaptic neurexins. J. Neurosci. 27 (2007) 2815-2824
71. Thibault S.T., Singer M.A., Miyazaki W.Y., Milash B., Dompe N.A., Singh C.M., Buchholz R., Demsky M., Fawcett R., Francis-Lang H.L., et al. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36 (2004) 283-287
72. Torroja L., Packard M., Gorczyca M., White K., and Budnik V. The Drosophila beta-amyloid precursor protein homolog promotes synapse differentiation at the neuromuscular junction. J. Neurosci. 19 (1999) 7793-7803
73. Ushkaryov Y.A., Petrenko A.G., Geppert M., and Sudhof T.C. Neurexins: synaptic cell surface proteins related to the alpha-latrotoxin receptor and laminin. Science 257 (1992) 50-56
74. Wagh D.A., Rasse T.M., Asan E., Hofbauer A., Schwenkert I., Durrbeck 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 49 (2006) 833-844
75. Yamagata M., Sanes J.R., and Weiner J.A. Synaptic adhesion molecules. Curr. Opin. Cell Biol. 15 (2003) 621-632
76. Yoshihara M., and Littleton J.T. Synaptotagmin I functions as a calcium sensor to synchronize neurotransmitter release. Neuron 36 (2002) 897-908
77. Zeng X., Sun M., Liu L., Chen F., Wei L., and Xie W. Neurexin-1 is required for synapse formation and larvae associative learning in Drosophila. FEBS Lett. 581 (2007) 2509-2516
78. Zhang W., Rohlmann A., Sargsyan V., Aramuni G., Hammer R.E., Sudhof T.C., and Missler M. Extracellular domains of alpha-neurexins participate in regulating synaptic transmission by selectively affecting N- and P/Q-type Ca2+ channels. J. Neurosci. 25 (2005) 4330-4342