Maturation of active zone assembly by Drosophila Bruchpilot

Journal of Cell Biology

Volumn 186, Issue 1, 2009, Pages 129-145

  Fouquet, Wernher ^a,b   Owald, David ^a,b   Wichmann, Carolin ^a,b   Mertel, Sara ^a   Depner, Harald ^a   Dyba, Marcus ^c   Hallermann, Stefan ^d   Kittel, Robert J ^b,d   Eimer, Stefan ^e   Sigrist, Stephan J ^a,b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c Leica Microsystems CMS GmbH   (Germany)

^d UNIVERSITY OF LEIPZIG   (Germany)

^e EUROPEAN NEUROSCIENCE INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; LIPRIN ALPHA; MEMBRANE PROTEIN; PROTEIN BRUCHPILOT; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; MOLECULAR INTERACTION; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STRUCTURE ACTIVITY RELATION; SYNAPSE VESICLE;

DROSOPHILA MELANOGASTER;

EID: 67650470999     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200812150     Document Type: Article

References (53)

1. Bellen, H.J., R.W. Levis, G. Liao, Y. He, J.W. Carlson, G. Tsang, M. Evans-Holm, P.R. Hiesinger, K.L. Schulze, G.M. Rubin, et al. 2004. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics. 167:761-781.
2. Brandstatter, J.H., S.R. Shaw, and I.A. Meinertzhagen. 1991. Terminal degeneration and synaptic disassembly following receptor photoablation in the retina of the fly's compound eye. J. Neurosci. 11:1930-1941.
3. Cao, Y.Q., E.S. Piedras-Renteria, G.B. Smith, G. Chen, N.C. Harata, and R.W. Tsien. 2004. Presynaptic Ca2+ channels compete for channel typepreferring slots in altered neurotransmission arising from Ca2+ channelopathy. Neuron. 43:387-400.
4. Catterall, W.A. 1998. Structure and function of neuronal Ca2+ channels and their role in neurotransmitter release. Cell Calcium. 24:307-323.
5. Catterall, W.A., and A.P. Few. 2008. Calcium channel regulation and presynaptic plasticity. Neuron. 59:882-901.
6. Collins, C.A., and A. DiAntonio. 2007. Synaptic development: insights from Drosophila. Curr. Opin. Neurobiol. 17:35-42.
7. Dai, Y., H. Taru, S.L. Deken, B. Grill, B. Ackley, M.L. Nonet, and Y. Jin. 2006. SYD-2 Liprin-alpha organizes presynaptic active zone formation through ELKS. Nat. Neurosci. 9:1479-1487.
8. Deguchi-Tawarada, M., E. Inoue, E. Takao-Rikitsu, M. Inoue, T. Ohtsuka, and Y. Takai. 2004. CAST2: identification and characterization of a protein structurally related to the presynaptic cytomatrix protein CAST. Genes Cells. 9:15-23.
9. Deguchi-Tawarada, M., E. Inoue, E. Takao-Rikitsu, M. Inoue, I. Kitajima, T. Ohtsuka, and Y. Takai. 2006. Active zone protein CAST is a component of conventional and ribbon synapses in mouse retina. J. Comp. Neurol. 495:480-496.
10. Evans, R.M., and G.W. Zamponi. 2006. Presynaptic Ca2+ channels-integration centers for neuronal signaling pathways. Trends Neurosci. 29:617-624.
11. Featherstone, D.E., E.M. Rushton, M. Hilderbrand-Chae, A.M. Phillips, F.R. Jackson, and K. Broadie. 2000. Presynaptic glutamic acid decarboxylase is required for induction of the postsynaptic receptor field at a glutamatergic synapse. Neuron. 27:71-84.
12. Feeney, C.J., S. Karunanithi, J. Pearce, C.K. Govind, and H.L. Atwood. 1998. Motor nerve terminals on abdominal muscles in larval flesh flies, Sarcophaga bullata: comparisons with Drosophila. J. Comp. Neurol. 402:197-209.
13. Frank, T., D. Khimich, A. Neef, and T. Moser. 2009. Mechanisms contributing to synaptic Ca2+ signals and their heterogeneity in hair cells. Proc. Natl. Acad. Sci. USA. 106:4483-4488.
14. Fuger, P., L.B. Behrends, S. Mertel, S.J. Sigrist, and T.M. Rasse. 2007. Live imaging of synapse development and measuring protein dynamics using two-color fluorescence recovery after photo-bleaching at Drosophila synapses. Nat. Protoc. 2:3285-3298.
15. Gray, N.W., R.M. Weimer, I. Bureau, and K. Svoboda. 2006. Rapid redistribution of synaptic PSD-95 in the neocortex in vivo. PLoS Biol. 4:e370.
16. Harlow, M.L., D. Ress, A. Stoschek, R.M. Marshall, and U.J. McMahan. 2001. The architecture of active zone material at the frog's neuromuscular junction. Nature. 409:479-484.
17. Hell, S.W. 2007. Far-field optical nanoscopy. Science. 316:1153-1158.
18. Hofbauer, A., T. Ebel, B. Waltenspiel, P. Oswald, Y.C. Chen, P. Halder, S. Biskup, U. Lewandrowski, C. Winkler, A. Sickmann, et al. 2009. The Wuerzburg hybridoma library against Drosophila brain. J. Neurogenet. 23:78-91.
19. Jin, Y., and C.C. Garner. 2008. Molecular mechanisms of presynaptic differentiation. Annu. Rev. Cell Dev. Biol. 24:237-262.
20. Kaufmann, N., J. DeProto, R. Ranjan, H. Wan, and D. Van Vactor. 2002. Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron. 34:27-38.
21. Kawasaki, F., R. Felling, and R.W. Ordway. 2000. A temperature-sensitive paralytic mutant defines a primary synaptic calcium channel in Drosophila. J. Neurosci. 20:4885-4889.
22. Kawasaki, F., S.C. Collins, and R.W. Ordway. 2002. Synaptic calcium-channel function in Drosophila: analysis and transformation rescue of temperaturesensitive paralytic and lethal mutations of cacophony. J. Neurosci. 22:5856-5864.
23. Kawasaki, F., B. Zou, X. Xu, and R.W. Ordway. 2004. Active zone localization of presynaptic calcium channels encoded by the cacophony locus of Drosophila. J. Neurosci. 24:282-285.
24. Kittel, R.J., C. Wichmann, T.M. Rasse, W. Fouquet, M. Schmidt, A. Schmid, D.A. Wagh, C. Pawlu, R.R. Kellner, K.I. Willig, et al. 2006. Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science. 312:1051-1054.
25. Ko, J., M. Na, S. Kim, J.R. Lee, and E. Kim. 2003. Interaction of the ERC family of RIM-binding proteins with the liprin-alpha family of multidomain proteins. J. Biol. Chem. 278:42377-42385.
26. Koh, Y.H., L.S. Gramates, and V. Budnik. 2000. Drosophila larval neuromuscular junction: molecular components and mechanisms underlying synaptic plasticity. Microsc. Res. Tech. 49:14-25.
27. Li, J., J. Ashley, V. Budnik, and M.A. Bhat. 2007. Crucial role of Drosophila neurexin in proper active zone apposition to postsynaptic densities, synaptic growth, and synaptic transmission. Neuron. 55:741-755.
28. Long, A.A., E. Kim, H.T. Leung, E. Woodruff III, L. An, R.W. Doerge, W.L. Pak, and K. Broadie. 2008. Presynaptic calcium channel localization and calcium-dependent synaptic vesicle exocytosis regulated by the Fuseless protein. J. Neurosci. 28:3668-3682.
29. Missler, M., W. Zhang, A. Rohlmann, G. Kattenstroth, R.E. Hammer, K. Gottmann, and T.C. Sudhof. 2003. Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature. 423:939-948.
30. Neher, E., and T. Sakaba. 2008. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron. 59:861-872.
31. Ohtsuka, T., E. Takao-Rikitsu, E. Inoue, M. Inoue, M. Takeuchi, K. Matsubara, M. Deguchi-Tawarada, K. Satoh, K. Morimoto, H. Nakanishi, and Y. Takai. 2002. Cast: a novel protein of the cytomatrix at the active zone of synapses that forms a ternary complex with RIM1 and munc13-1. J. Cell Biol. 158:577-590.
32. Owald, D., and S.J. Sigrist. 2009. Assembling the presynaptic active zone. Curr. Opin. Neurobiol. doi:10.1016/j.conb.2009.03.003.
33. Parks, A.L., K.R. Cook, M. Belvin, N.A. Dompe, R. Fawcett, K. Huppert, L.R. Tan, C.G. Winter, K.P. Bogart, J.E. Deal, et al. 2004. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36:288-292.
34. Patel, M.R., E.K. Lehrman, V.Y. Poon, J.G. Crump, M. Zhen, C.I. Bargmann, and K. Shen. 2006. Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat. Neurosci. 9:1488-1498.
35. Prokop, A., and I.A. Meinertzhagen. 2006. Development and structure of synaptic contacts in Drosophila. Semin. Cell Dev. Biol. 17:20-30.
36. Qin, G., T. Schwarz, R.J. Kittel, A. Schmid, T.M. Rasse, D. Kappei, E. Ponimaskin, M. Heckmann, and S.J. Sigrist. 2005. Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila. J. Neurosci. 25:3209-3218.
37. Rasse, T.M., W. Fouquet, A. Schmid, R.J. Kittel, S. Mertel, C.B. Sigrist, M. Schmidt, A. Guzman, C. Merino, G. Qin, et al. 2005. Glutamate receptor dynamics organizing synapse formation in vivo. Nat. Neurosci. 8:898-905.
38. Rostaing, P., E. Real, L. Siksou, J.P. Lechaire, T. Boudier, T.M. Boeckers, F. Gertler, E.D. Gundelfinger, A. Triller, and S. Marty. 2006. Analysis of synaptic ultrastructure without fixative using high-pressure freezing and tomography. Eur. J. Neurosci. 24:3463-3474.
39. Rybak, J., and I.A. Meinertzhagen. 1997. The effects of light reversals on photoreceptor synaptogenesis in the fly Musca domestica. Eur. J. Neurosci. 9:319-333.
40. Schmid, A., G. Qin, C. Wichmann, R.J. Kittel, S. Mertel, W. Fouquet, M. Schmidt, M. Heckmann, and S.J. Sigrist. 2006. Non-NMDA-type glutamate receptors are essential for maturation but not for initial assembly of synapses at Drosophila neuromuscular junctions. J. Neurosci. 26:11267-11277.
41. Schmid, A., S. Hallermann, R.J. Kittel, O. Khorramshahi, A.M. Frolich, C. Quentin, T.M. Rasse, S. Mertel, M. Heckmann, and S.J. Sigrist. 2008. Activity-dependent site-specific changes of glutamate receptor composition in vivo. Nat. Neurosci. 11:659-666.
42. Schoch, S., and E.D. Gundelfinger. 2006. Molecular organization of the presynaptic active zone. Cell Tissue Res. 326:379-391.
43. Sigrist, S.J., D.F. Reiff, P.R. Thiel, J.R. Steinert, and C.M. Schuster. 2003. Experience-dependent strengthening of Drosophila neuromuscular junctions. J. Neurosci. 23:6546-6556.
44. Siksou, L., P. Rostaing, J.P. Lechaire, T. Boudier, T. Ohtsuka, A. Fejtova, H.T. Kao, P. Greengard, E.D. Gundelfinger, A. Triller, and S. Marty. 2007. Three-dimensional architecture of presynaptic terminal cytomatrix. J. Neurosci. 27:6868-6877.
45. Stryker, E., and K.G. Johnson. 2007. LAR, liprin alpha and the regulation of active zone morphogenesis. J. Cell Sci. 120:3723-3728.
46. tom Dieck, S., W.D. Altrock, M.M. Kessels, B. Qualmann, H. Regus, D. Brauner, A. Fejtova, O. Bracko, E.D. Gundelfinger, and J.H. Brandstatter. 2005. Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J. Cell Biol. 168:825-836.
47. Wagh, D.A., T.M. Rasse, E. Asan, A. Hofbauer, I. Schwenkert, H. Durrbeck, S. Buchner, M.C. Dabauvalle, M. Schmidt, G. Qin, et al. 2006. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron. 49:833-844.
48. Wang, Y., X. Liu, T. Biederer, and T.C. Sudhof. 2002. A family of RIM-binding proteins regulated by alternative splicing: implications for the genesis of synaptic active zones. Proc. Natl. Acad. Sci. USA. 99:14464-14469.
49. Westphal, V., S.O. Rizzoli, M.A. Lauterbach, D. Kamin, R. Jahn, and S.W. Hell. 2008. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science. 320:246-249.
50. Wojtowicz, J.M., L. Marin, and H.L. Atwood. 1994. Activity-induced changes in synaptic release sites at the crayfish neuromuscular junction. J. Neurosci. 14:3688-3703.
51. Wucherpfennig, T., M. Wilsch-Brauninger, and M. Gonzalez-Gaitan. 2003. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol. 161:609-624.
52. Zeng, X., M. Sun, L. Liu, F. Chen, L. Wei, and W. Xie. 2007. Neurexin-1 is required for synapse formation and larvae associative learning in Drosophila. FEBS Lett. 581:2509-2516.
53. Zhai, R.G., and H.J. Bellen. 2004. The architecture of the active zone in the presynaptic nerve terminal. Physiology (Bethesda). 19:262-270.