Skip to main content
Log in

Presynaptic proteins involved in exocytosis inDrosophila melanogaster: A genetic analysis

  • Review
  • Published:
Invertebrate Neuroscience

Abstract

Neuronal communication involves the fusion of neurotransmitter filled synaptic vesicles with the presynaptic terminal. This exocytotic event depends upon proteins present in three separate compartments: the synaptic vesicle, the synaptic cytosol, and the presynaptic membrane. Recent data indicate that the basic components of exocytotic pathways, including those used for neurotransmitter release, are conserved from yeast to human. Genetic dissection of the secretory pathway in yeast, identification of the target proteins cleaved by the clostridial neurotoxins and biochemical characterization of the interactions of synaptic proteins from vertebrates have converged to provide the SNARE (soluble NSF attachment protein receptor) hypothesis for vesicle trafficking. This model proposes that proteins present in the vesicle (v-SNAREs) interact with membrane receptors (t-SNAREs) to provide a molecular scaffold for cytosolic proteins involved in fusion. The hypothesis that these mechanisms function at the synapse relies largely uponin vitro evidence. Recently, genetic approaches in mice, C.elegans and the fruitfly,Drosophila melanagaster, have been used to dissect thein vivo function of numerous proteins involved in synaptic transmission. This review covers recent progress and insights provided by a genetic dissection of neurotransmitter release inDrosophila. In addition, we will provide evidence that the mechanisms for synaptic communication are highly conserved from invertebrates to vertebrates, makingDrosophila an ideal model system to further unravel the intricacies of synaptic transmission.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aalto, M. K., Keranen, S., and Ronne, H. (1992) A family of proteins involved in intracellular sorting.Cell,68, 181–182.

    Article  CAS  PubMed  Google Scholar 

  • Aalto, M. K., Ronne, H. and Keranen, S. (1993) Yeast syntaxins Sso1p and Sso2p belong to a family of related membrane proteins that function in vesicular transport.EMBO J.,12, 4095–4104.

    CAS  PubMed  Google Scholar 

  • Atkinson, N. S., Robertson, G. A. and Ganetsky, B. (1991) A component of calcium-activated potassium channels encoded by theDrosophila slo locus.Science,253, 551–555.

    CAS  PubMed  Google Scholar 

  • Beckingham, K., Doyle, K. E. and Maune, J. F. (1987) The calmodulin gene ofDrosophila melanogaster.Methods Enzymol.,139, 230–247.

    CAS  PubMed  Google Scholar 

  • Bennett, M. K., Calakos, N. and Schellet, R. H. (1992) Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones.Science,257, 255–259.

    CAS  PubMed  Google Scholar 

  • Bennett, M. K. and Scheller, R. H. (1993) The molecular machinery for secretion is conserved from yeast to neurons.Proc. Nad. Acad. Sci. USA,90, 2559–2563.

    CAS  Google Scholar 

  • Bennett, M. K., Garcia-Arraras, J. E., Elferink, L. A., Peterson, K., Fleming, A. M., Hazuka, C. D. and Scheller, R. H. (1993) The syntaxin family of vesicular transport receptors.Cell,74, 863–873.

    CAS  PubMed  Google Scholar 

  • Blasi, J., Chapman, E. R., Link, E., Binz, T., Yamasaki, S., DeCamilli, P., Südhof, T. C., Niemann, H. and Jahn, R. (1993a) Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25.Nature,365, 160–163.

    Article  CAS  PubMed  Google Scholar 

  • Blasi, J., Chapman, E. R., Yamaski, S., Binz, T., Niemann, H. and Jahn, R. (1993b) Botulinum neurotoxin C1 blocks neurotransmitter release by means of cleaving HPC-1/syntaxin.EMBO J.,12, 4821–4828.

    CAS  PubMed  Google Scholar 

  • Block, M. R., Glick, B. S., Wilcox, D. A., Wieland, F. T. and Rothman, J. E. (1988) Purification of an N-ethylmaleimidesensitive protein catalyzing vesicular transport.Proc. Natl. Acad. Sci. USA,85, 7852–7856.

    CAS  PubMed  Google Scholar 

  • Brennwald, P., Kearns, B., Champion, K., Keranen, S., Bankaitis, V. and Novick, P. (1994) Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis.Cell,79, 245–258.

    Article  CAS  PubMed  Google Scholar 

  • Broadie, K. S. and Bate, M. (1993) Development of the embryonic neuromuscular synapse ofDrosophila melanogaster.J. Neurosci.,13, 144–166.

    CAS  PubMed  Google Scholar 

  • Broadie, K. S., Bellen, H. J., DiAntonio, A., Littleton, J. T. and Schwarz, T. L. (1994) The absence of synaptotagmin disrupts excitation-secretion coupling during synaptic transmission.Proc. Natl. Acad. Sci. USA,91, 10727–10731.

    CAS  PubMed  Google Scholar 

  • Bruggeman, A., Pardo, L. A., Stuhmer, W. and Pongs, O. (1993)Ether-a-go-go encodes a voltage gated channel permeable to K+ and Ca++ and modulated by cAMP.Nature,365, 445–448.

    Google Scholar 

  • Butler, A., Wei, A., Baker, K. and Salkoff, L. (1989) A family of putative potassium channel genes inDrosophila.Science,243, 943–947.

    CAS  PubMed  Google Scholar 

  • Chin, A. C., Burgess, R. W., Wong, B. R., Schwarz, T. L. and Scheller, R. H. (1993) Differential expression of transcripts fromsyb, aDrosophila melanogaster gene encoding VAMP (synaptobrevin) that is abundant in non-neuronal cells.Gene,131, 175–181.

    Article  CAS  PubMed  Google Scholar 

  • Clary, D. O., Griff, I. C. and Rothman, J. E. (1990) SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast.Cell,61, 709–721.

    Article  CAS  PubMed  Google Scholar 

  • Davis, R. L. and Davidson, N. (1984) Isolation of theDrosophila melanogaster dunce chromosomal region and recombinational mapping ofdunce sequences with restriction site polymorphisms as genetic markers.Mol. Cell Biol.,4, 358–367.

    CAS  PubMed  Google Scholar 

  • DiAntonio, A., Burgess, R. W., Chin, A. C., Deitcher, D. L., Scheller, R. H. and Schwarz, T. L. (1993a) Identification and characterization ofDrosophila genes for synaptic vesicle proteins.J. Neurosci.,13, 4924–4935.

    CAS  PubMed  Google Scholar 

  • DiAntonio, A., Parfitt, K. D. and Schwarz, T. L. (1993b) Synaptic transmission persists insynaptotagmin mutants ofDrosophila.Cell,73, 1281–1290.

    Article  CAS  PubMed  Google Scholar 

  • DiAntonio, A. and Schwarz, T.L. (1994) The effect on synaptic physiology ofsynaptotagmin mutations inDrosophila.Neuron,12, 909–920.

    Article  CAS  PubMed  Google Scholar 

  • Fisher von Mollard, G., Südhof, T. C. and Jahn, R. (1991) A small GTP-binding protein dissociates from synaptic vesicles during exocytosis.Nature,349, 79–81.

    Google Scholar 

  • Fournier, D., Karch, F., Bride, J. M., Hall, L. M., Berge, J. B. and Spierer, P. (1989)Drosophila melanogaster acetylcholinesterase gene: structure, evolution and mutations.J. Mol. Biol.,210, 15–22.

    Article  CAS  PubMed  Google Scholar 

  • Garcia, E. P., Gatti, E., Butler, M., Burton, J. and DeCamilli, P. (1994) A rat brain Secl homologue related to Rop and UNC-18 interacts with syntaxin.Proc. Natl. Acad. Sci. USA,91, 2003–2007.

    CAS  PubMed  Google Scholar 

  • Gengyo-Ando, K., Kamiya, Y., Yamakawa, A., Kodaira, K.-i., Nishiwaki, K., Miwa, J., Hori, I. and Hosono, R. (1993) The C.elegans unc-18 gene encodes a protein expressed in motor neurons.Neuron,11, 703–711.

    Article  CAS  PubMed  Google Scholar 

  • Geppert, M., Bolshakov, V. Y., Siegelbaum, S. A., Takei, K., DeCamilli, P., Hammer, R. E. and Südhof, T. C. (1994) The role of rab3a in neurotransmitter release.Nature,369, 493–497.

    Article  CAS  PubMed  Google Scholar 

  • Griff, I. C., Schekman, R., Rothman, J. E. and Kaiser, C. A. (1992) The yeast Sec 17 gene product is functionally equivalent to mammalian α-SNAP protein.J. Biol. Chem.,267, 12106–12115.

    CAS  PubMed  Google Scholar 

  • Gundersen, C. B. and Umbach, J. A. (1992) Suppression cloning of the cDNA encoding a candidate subunit of a presynaptic calcium channel.Neuron,9, 527–537.

    Article  CAS  PubMed  Google Scholar 

  • Hardwick, K. G. and Pelham, H. R. B. (1992) SED5 encodes a 39 kDa integral membrane protein requred for vesicular transport between the ER and Golgi complex.J. Cell Biol.,119, 513–521.

    Article  CAS  PubMed  Google Scholar 

  • Harrison, S. D., Broadie, K., van de Goor, J. and Rubin, G. M. (1994) Mutations in theDrosophila Rop gene suggest a function in general secretion and synaptic transmission.Neuron,13, 555–566.

    Article  CAS  PubMed  Google Scholar 

  • Hata, Y., Slaughter, C. A. and Südhof, T. C. (1993) Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin.Nature,366, 347–351.

    Article  CAS  PubMed  Google Scholar 

  • Heimbeck, G., Klagges, B., Pfludfelder, G. O., Reifegerste, R., Hoflouer, A., Büchner, S. and Buchner, E. (1991) A gene selectively expressed in the brain ofDrosophila encodes a protein with partial homology to vertebrate synapsin I.Europ. Dros. Res. Conf.,12, 236.

    Google Scholar 

  • Hunt, J. M., Charlton, M. P., Kistner, A., Habermann, E., Augustine, G. J. and Betz, H. (1994) A post-docking role for synaptobrevin in synaptic vesicle fusion.Neuron,12, 1269–1279.

    Article  CAS  PubMed  Google Scholar 

  • Itoh, N., Slemmon, J. R., Hawke, D. H., Williamson, R., Morita, E., Itakura, K., Roberts, E., Shively, J. E., Crawford, G. D. and Salvaterra, P. M. (1986) Cloning ofDrosophila choline acetyltransferase cDNA.Proc. Natl. Acad. Sci. USA,83, 4081–4085.

    CAS  PubMed  Google Scholar 

  • Jan, L. Y. and Jan, Y. N. (1976). Properties of the larval neuromuscular junction inDrosophila melanogaster.J. Physiol. (Lond),262, 189–214.

    CAS  Google Scholar 

  • Johnston, P. A., Archer, B. T., Robinson, K., Mignery, G. A., Jahn, R. and Südhof, T. C. (1991) Rab3a attachment to synaptic vesicle membrane mediated by a conserved polyisoprenylated carboxy-terminal sequence.Neuron,7, 101–109.

    Article  CAS  PubMed  Google Scholar 

  • Kaibuchi, K., Fukumoto, Y., Oku, N., Takai, Y., Arai, K. and Muramatsu, M. (1989) Molecular and genetic analysis of the regulatory and catalytic domains of protein kinase C.J. Biol. Chem.,264, 13489–13496.

    CAS  PubMed  Google Scholar 

  • Kamb, A., Iverson, L. E. and Tanouye, M. A. (1987) Molecular characterization ofShaker, aDrosophila gene that encodes a potassium channel.Cell,50, 405–413.

    Article  CAS  PubMed  Google Scholar 

  • Katz, B. (1969)The release of neural transmitter substances. Liverpool: Liverpool University Press.

    Google Scholar 

  • Kousky, C., Ren, D. and Hall, L. M. (1994) Identification and characterization of aDrosophila calcium channel Β subunit.Dros. Res. Conf. Absts.,35, 81.

    Google Scholar 

  • Levin, L. R., Han, P.-L., Hwang, P. M., Feinstein, P. G., Davis, R. L. and Reed R. R. (1992) TheDrosophila learning and memory generutabaga encodes a Ca++/calmodulin responsive adenylyl cyclase.Cell,68, 479–489.

    Article  CAS  PubMed  Google Scholar 

  • Littleton, J. T., Bellen, H. J. and Perin, M. S. (1993a) Expression of synaptotagmin inDrosophila reveals transport and localization of synaptic vesicles to the synapse.Development,118, 1077–1088.

    CAS  PubMed  Google Scholar 

  • Littleton, J. T., Stern, M., Schulze, K., Perin, M. and Bellen, H. J. (1993b) Mutational analysis ofDrosophila synaptotagmin demonstrates its essential role in Ca++-activated neurotransmitter release.Cell,74, 1125–1134.

    Article  CAS  PubMed  Google Scholar 

  • Littleton, J. T., Stern, M., Perin, M., and Bellen, H. J. (1994) Calcium dependence of neurotransmitter release and rate of spontaneous vesicle fusions are altered inDrosophila synaptotagmin mutations.Proc. Natl. Acad. Sci. USA,91, 10888–10892.

    CAS  PubMed  Google Scholar 

  • Littleton, J. T. and Bellen, H. J. (1994) Genetic and phenotypic analysis of 13 essential genes in cytological interval 22F1-2; 23B1-2 reveals novel genes required for neuronal development inDrosophila.Genetics,138, 111–123.

    CAS  PubMed  Google Scholar 

  • Littleton, J. T., Upton, L. and Kania, A. (1995) Immunocytochemical analysis of axonal outgrowth insynaptotagmin mutations.J. Neurochem.,65, in press.

  • Loughney, K., Kreber, R., and Ganetzky, B. (1989) Molecular analysis of thepara locus, a sodium channel gene inDrosophila.Cell,58, 1143–1154.

    Article  CAS  PubMed  Google Scholar 

  • Mastrogiacomo, A., Parsons, S. M., Zampighi, G. A., Jenden, D. J., Umbach, J. A. and Gunderson, C. B. (1994) Cysteine string proteins: a potential link between synaptic vesicles and presynaptic calcium channels.Science,263, 981–982.

    CAS  PubMed  Google Scholar 

  • Nishizuka, Y. (1989) The family of protein kinase C for signal transduction.JAMA,262, 1826–1833.

    Article  CAS  PubMed  Google Scholar 

  • Nonet, M. L., Grundahl, K., Meyer, B. J. and Rand, J. B. (1993) Synaptic function is impaired but not eliminated in C.elegans mutants lacking synaptotagmin.Cell,73, 1291–1305.

    Article  CAS  PubMed  Google Scholar 

  • Ordway, R. W., Pallanck, L. and Ganetzky, B. (1994) Neurally expressedDrosophila genes encoding homologs of the NSF and SNAP secretory proteins.Proc. Natl. Acad. Sci. USA,91, 5715–5719.

    CAS  PubMed  Google Scholar 

  • Oyler, G. A., Higgins, G. A., Hart, R. A., Battenberg, E., Billingsley, M., Bloom, F. E. and Wilson, M. C. (1989) The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations.J. Cell Biol.,109, 3039–3052.

    Article  CAS  PubMed  Google Scholar 

  • Papazian, D. M., Schwarz, T. L., Tempel, B. L., Jan, Y. N. and Jan, L. Y. (1987) Cloning of genomic and complementary DNA fromShaker, a putative potassium channel gene fromDrosophila.Science,237, 749–753.

    CAS  PubMed  Google Scholar 

  • Perin, M. S., Fried, V. A., Mignery, G. A., Jahn, R. and Südhof, T.C. (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory domain of protein kinase C.Nature,345, 260–263.

    Article  CAS  PubMed  Google Scholar 

  • Perin, M. S., Johnston, P. A., Ozcelik, T., Jahn, R., Francke, U. and Südhof, T. C. (1991) Structural and functional conservation of synaptotagmin (p65) inDrosophila and humans.J. Biol. Chem.,266, 615–622.

    CAS  PubMed  Google Scholar 

  • Perin, M.S. (1994) The COOH-terminus of synaptotagmin mediates interaction with the neurexins.J. Biol. Chem.,269, 8576–8581.

    CAS  PubMed  Google Scholar 

  • Petrenko, A. G., Perin, M. S., Davletov, B. A., Ushkaryov, Y. A., Geppert, M. and Südhof, T. C. (1991) Binding of synaptotagmin to the α-latrotoxin receptor implicates both in synaptic vesicle exocytosis.Nature,353, 65–68.

    Article  CAS  PubMed  Google Scholar 

  • Pevsner, J., Hsu, S.-C. and Scheller, R. (1994a) n-Sec1: a neuralspecific syntaxin-binding protein.Proc. Natl. Acad. Sci. USA,91, 1445–1449.

    CAS  PubMed  Google Scholar 

  • Pevsner, J., Hsu, S.-C., Braun, J. E. A., Calakos, N., Ting, A. E., Bennett, M. K. and Scheller, R. H. (1994b) Specificity and regulation of a synaptic vesicle docking complex.Neuron,13, 353–361.

    Article  CAS  PubMed  Google Scholar 

  • Pongs, O., Lindemeier, J., Zhu, X. R., Theil, T., Engelkamp, D., Krah-Jentgens, I., Lambrecht, H. G., Koch, K. W., Schwemer, J., Rivosecchi, R., Mallart, A., Galceran, J., Canal, I., Barbas, J. A. and Ferrus, A. (1993) Frequenin—A novel calcium-binding protein that modulates synaptic efficacy in theDrosophila nervous system.Neuron,11, 15–28.

    Article  CAS  PubMed  Google Scholar 

  • Protopopov, V., Govindav, B., Novick, P. and Gerst, J. E. (1993) Homologs of the synaptobrevin/VAMP family of synaptic vesicle proteins function in the late secretory pathway in S.cerevisiae.Cell,74, 855–861.

    Article  CAS  PubMed  Google Scholar 

  • Risinger, C., Blomqvist, A. G., Lundell, I., Lambertsson, A., Nassel, D., Pieribone, V. A., Brodin, L. and Larhammar, D. (1993) Evolutionary conservation of synaptosome-associated protein 25 kDa (SNAP-25) shown byDrosophila andTorpedo cDNA clones.J. Biol. Chem.,268, 24408–24414.

    CAS  PubMed  Google Scholar 

  • Rivosecchi, R., Pongs, O. and Mallart, A. (1994) Implication of frequenin in the facilitation of transmitter release inDrosophila.J. Physiol. (Lond),474, 223–231.

    CAS  Google Scholar 

  • Salkoff, L., Butler, A., Wei, A., Scavarda, N., Giffen, K., Ifune, C., Goodman, R. and Mandel, G. (1987) Genomic organization and deduced amino acid sequence of a putative sodium channel gene inDrosophila.Science,237, 744–749.

    CAS  PubMed  Google Scholar 

  • Salmimen, A. and Novick, P.J. (1987) A ras like protein is required for a post-Golgi event in yeast secretion.Cell,49, 527–538.

    Google Scholar 

  • Salzberg, A., Cohen, N., Halachmi, N., Kimchie, Z. and Lev, Z. (1993) TheDrosophila Ras2 andRop gene pair: a dual homology with a yeastRas-like gene and a suppressor of its loss-of-function phenotype.Development,117, 1309–1319.

    CAS  PubMed  Google Scholar 

  • Schiavo, G., Benfenati, F., Poulain, B., Rossetto, O., Polverino de Laureto, P., DasGupta, B. R. and Montecucco, C. (1992) Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteotytic cleavage of synaptobrevin.Nature,359, 832–835.

    Article  CAS  PubMed  Google Scholar 

  • Schulze, K. L., Littleton, J. T., Salzberg, A., Halachmi, N., Stern, M., Lev, Z. and Bellen, H. J. (1994). The rop protein, aDrosophila homolog of the vertebrate n-Sec1/Munc18 and yeast Secl proteins, is a negative regulator of neurotransmitter release in vivo.Neuron,13, 1099–1108.

    Article  CAS  PubMed  Google Scholar 

  • Schulze, K. L., Broadie, K., Perin, M. S. and Bellen, H. J. (1995). Genetic and electrophysiological studies ofDrosophila syntaxin-1A demonstrate its role in non-neuronal secretion and its essential role in neurotransmitter release.Cell,80, 311–320.

    Article  CAS  PubMed  Google Scholar 

  • Segev, N. Mulhollard, J. and Botstein, D. (1988). The yeast GTP-binding protein Ypt1 protein and a mammalian counterpart are associated with the secretion machinery.Cell,52, 915–924.

    Article  CAS  PubMed  Google Scholar 

  • Shirataki, H., Kaibuchi, K., Sakoda, T., Kishida, S., Yamaguchi, T., Wada, K., Miyazaki, M. and Takai, Y. (1993). Rabphilin-3A, a putative target protein for smg p25a/rab3a p25 small GTP-binding protein related to synaptotagmin.Mol. Cell. Biol.,13, 2061–2068.

    CAS  PubMed  Google Scholar 

  • Söllner, T., Whiteheart, S. W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P. and Rothman, J. E. (1993a). SNAP receptors implicated in vesicle targeting and fusion.Nature,362, 318–324.

    Article  PubMed  Google Scholar 

  • Söllner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. and Rothman, J. E. (1993b) A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion.Cell,75, 409–418.

    PubMed  Google Scholar 

  • Stern, M. and Ganetzky, B. (1989) Altered synaptic transmission inDrosophila Hyperkinetic mutants.J. Neurogenet.,5, 215–228.

    CAS  PubMed  Google Scholar 

  • Stern, M. and Ganetzky, B. (1992). Identification and characterization ofinebriated, a gene affecting neuronal excitability inDrosophila.J. Neurogenet.,8, 157–172.

    CAS  PubMed  Google Scholar 

  • Südhof, T. C., Baumert, M., Perin, M. S. and Jahn, R. (1989) A synaptic vesicle membrane protein is conserved from mammals toDrosophila.Neuron,2, 1475–1481.

    PubMed  Google Scholar 

  • Sweeney, S. T., Broadie, K., Keane, J., Niemann, H. and O'Kane, C. J. (1995) Targeted expression of tetanus toxin light chain inDrosophila specifically eliminates synaptic transmission and causes behavioural defects.Neuron,14, 341–351.

    Article  CAS  PubMed  Google Scholar 

  • Trimble, W. S., Cowna, D. M. and Scheller, R. H. (1988) Vamp-1: a synaptic vesicle-associated integral membrane protein.Proc. Natl. Acad. Sci. USA,85, 4538–4552.

    CAS  PubMed  Google Scholar 

  • Umbach, J. A., Zinsmaier, K. E., Eberle, K. K., Büchner, E., Benzer, S. and Gundersen, C. B. (1994) Presynaptic dysfunction inDrosophila csp mutants.Neuron,13, 899–907.

    Article  CAS  PubMed  Google Scholar 

  • Ushkaryov, Y. A., Petrenko, A. G., Geppert, M. and Südhof, T. C. (1992). Neurexins: synaptic cell surface proteins related to the α-latrotoxin receptor and laminin.Science,257, 50–56.

    CAS  PubMed  Google Scholar 

  • van der Bliek, A. M. and Meyerowitz, E. M. (1991) Dynamin-like protein encoded by theDrosophila shibire gene associated with vesicular traffic.Nature,351, 411–414.

    PubMed  Google Scholar 

  • Warmke, J., Drysdale, R. and Ganetzky, B. (1991) A distinct potassium channel polypeptide encoded by theDrosophila eag locus.Science,252, 1560–1562.

    CAS  PubMed  Google Scholar 

  • Wilson, D. W., Whiteheart, S. W., Wiedman, M., Brunner, M. and Rothman, J. E. (1992) A multisubunit particle implicated in membrane fusion.J. Cell Biol.,117, 531–538.

    Article  CAS  PubMed  Google Scholar 

  • Wu, C-F. and Ganetzky, B. (1992) Neurogenetic studies of ion channels inDrosophila. InIon Channels Volume 3, ed. T. Narahashi, pp. 261–314. New York: Plenum Press.

    Google Scholar 

  • Zhang, J. Z., Davletov, B. A., Südhof, T. C. and Anderson, R. G. (1994) Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling.Cell,78, 751–760.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, W., Feng, G., Ren, D., Eberl, D. F., Hannan, F., Dubald, M. and Hall, L. M. (1995) Cloning and characterization of a calcium channel α1 subunit fromDrosophila melanogaster with similarity to the rat brain type D isoform.J. Neurosci.,15, 1132–1143.

    CAS  PubMed  Google Scholar 

  • Zinsmaier, K., Holfauer, A., Heimbeck, G., Pflugfelder, G. O., Buchner, S. and Buchner, E. (1990) A cysteine-string protein is expressed in retina and brain ofDrosophila.J. Neurogenet.,7, 15–29.

    CAS  PubMed  Google Scholar 

  • Zinsmaier, K. E., Eberle, K. K., Buchner, E., Walter, N. and Benzer, S. (1994) Paralysis and early death in cysteine string protein mutants ofDrosophila.Science,263, 977–980.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Littleton, J.T., Bellen, H.J. Presynaptic proteins involved in exocytosis inDrosophila melanogaster: A genetic analysis. Invertebrate Neuroscience 1, 3–13 (1995). https://doi.org/10.1007/BF02331827

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02331827

Key words

Navigation