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. 1996 Dec;144(4):1713–1724. doi: 10.1093/genetics/144.4.1713

Drosophila Syntaxin Is Required for Cell Viability and May Function in Membrane Formation and Stabilization

K L Schulze 1, H J Bellen 1
PMCID: PMC1207721  PMID: 8978057

Abstract

The role of the Drosophila homologue of syntaxin-1A (syx) in neurotransmission has been extensively studied. However, developmental Northern analyses and in situ hybridization experiments show that SYX mRNA is expressed during all stages and in many tissues. We have isolated new mutations in syx that reveal roles for syx outside the nervous system. In the ovary, SYX is present in the germarium, but it is predominantly localized to nurse cell membranes. Mitotic recombination experiments in the germ-line show SYX is essential for oogenesis and may participate in membrane biogenesis in the nurse cells. In the early embryo, a large contribution of maternally deposited RNA is present, and the protein is localized at cell membranes during cellularization. After the maternal contribution is depleted, zygotically produced SYX assists secretion events occurring late in embryogenesis, such as cuticle deposition and neurotransmitter release. However, SYX is also required in larval imaginal discs, as certain hypomorphic mutant combinations exhibit rough eyes and wing notch defects indicative of cell death. Furthermore, recombinant clones that lack syx cause cell lethality in the developing eye. We propose that, similar to its roles in cuticle secretion and neurotransmitter release, SYX may mediate membrane assembly events throughout Drosophila development.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bennett M. K., Calakos N., Scheller R. H. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science. 1992 Jul 10;257(5067):255–259. doi: 10.1126/science.1321498. [DOI] [PubMed] [Google Scholar]
  2. Bennett M. K., Scheller R. H. The molecular machinery for secretion is conserved from yeast to neurons. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2559–2563. doi: 10.1073/pnas.90.7.2559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bezprozvanny I., Scheller R. H., Tsien R. W. Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature. 1995 Dec 7;378(6557):623–626. doi: 10.1038/378623a0. [DOI] [PubMed] [Google Scholar]
  4. Broadie K., Prokop A., Bellen H. J., O'Kane C. J., Schulze K. L., Sweeney S. T. Syntaxin and synaptobrevin function downstream of vesicle docking in Drosophila. Neuron. 1995 Sep;15(3):663–673. doi: 10.1016/0896-6273(95)90154-x. [DOI] [PubMed] [Google Scholar]
  5. Calakos N., Bennett M. K., Peterson K. E., Scheller R. H. Protein-protein interactions contributing to the specificity of intracellular vesicular trafficking. Science. 1994 Feb 25;263(5150):1146–1149. doi: 10.1126/science.8108733. [DOI] [PubMed] [Google Scholar]
  6. Cerezo J. R., Jiménez F., Moya F. Characterization and gene cloning of Drosophila syntaxin 1 (Dsynt1): the fruit fly homologue of rat syntaxin 1. Brain Res Mol Brain Res. 1995 Apr;29(2):245–252. doi: 10.1016/0169-328x(94)00254-c. [DOI] [PubMed] [Google Scholar]
  7. Chapman E. R., Hanson P. I., An S., Jahn R. Ca2+ regulates the interaction between synaptotagmin and syntaxin 1. J Biol Chem. 1995 Oct 6;270(40):23667–23671. doi: 10.1074/jbc.270.40.23667. [DOI] [PubMed] [Google Scholar]
  8. Chou T. B., Perrimon N. Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics. 1992 Jul;131(3):643–653. doi: 10.1093/genetics/131.3.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ferro-Novick S., Jahn R. Vesicle fusion from yeast to man. Nature. 1994 Jul 21;370(6486):191–193. doi: 10.1038/370191a0. [DOI] [PubMed] [Google Scholar]
  10. Foe V. E., Alberts B. M. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci. 1983 May;61:31–70. doi: 10.1242/jcs.61.1.31. [DOI] [PubMed] [Google Scholar]
  11. Fujita S. C., Zipursky S. L., Benzer S., Ferrús A., Shotwell S. L. Monoclonal antibodies against the Drosophila nervous system. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7929–7933. doi: 10.1073/pnas.79.24.7929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fullilove S. L., Jacobson A. G. Nuclear elongation and cytokinesis in Drosophila montana. Dev Biol. 1971 Dec;26(4):560–577. doi: 10.1016/0012-1606(71)90141-2. [DOI] [PubMed] [Google Scholar]
  13. Hanson P. I., Otto H., Barton N., Jahn R. The N-ethylmaleimide-sensitive fusion protein and alpha-SNAP induce a conformational change in syntaxin. J Biol Chem. 1995 Jul 14;270(28):16955–16961. doi: 10.1074/jbc.270.28.16955. [DOI] [PubMed] [Google Scholar]
  14. Harrison S. D., Broadie K., van de Goor J., Rubin G. M. Mutations in the Drosophila Rop gene suggest a function in general secretion and synaptic transmission. Neuron. 1994 Sep;13(3):555–566. doi: 10.1016/0896-6273(94)90025-6. [DOI] [PubMed] [Google Scholar]
  15. Hata Y., Slaughter C. A., Südhof T. C. Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature. 1993 Nov 25;366(6453):347–351. doi: 10.1038/366347a0. [DOI] [PubMed] [Google Scholar]
  16. Hayashi T., McMahon H., Yamasaki S., Binz T., Hata Y., Südhof T. C., Niemann H. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J. 1994 Nov 1;13(21):5051–5061. doi: 10.1002/j.1460-2075.1994.tb06834.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ingham P. W., Taylor A. M., Nakano Y. Role of the Drosophila patched gene in positional signalling. Nature. 1991 Sep 12;353(6340):184–187. doi: 10.1038/353184a0. [DOI] [PubMed] [Google Scholar]
  18. Jahn R., Niemann H. Molecular mechanisms of clostridial neurotoxins. Ann N Y Acad Sci. 1994 Sep 15;733:245–255. doi: 10.1111/j.1749-6632.1994.tb17274.x. [DOI] [PubMed] [Google Scholar]
  19. Kee Y., Lin R. C., Hsu S. C., Scheller R. H. Distinct domains of syntaxin are required for synaptic vesicle fusion complex formation and dissociation. Neuron. 1995 May;14(5):991–998. doi: 10.1016/0896-6273(95)90337-2. [DOI] [PubMed] [Google Scholar]
  20. Littleton J. T., Bellen H. J., Perin M. S. Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse. Development. 1993 Aug;118(4):1077–1088. doi: 10.1242/dev.118.4.1077. [DOI] [PubMed] [Google Scholar]
  21. Lukowitz W., Mayer U., Jürgens G. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell. 1996 Jan 12;84(1):61–71. doi: 10.1016/s0092-8674(00)80993-9. [DOI] [PubMed] [Google Scholar]
  22. Müller H. P., Schaffner W. Transcriptional enhancers can act in trans. Trends Genet. 1990 Sep;6(9):300–304. doi: 10.1016/0168-9525(90)90236-y. [DOI] [PubMed] [Google Scholar]
  23. Novick P., Field C., Schekman R. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell. 1980 Aug;21(1):205–215. doi: 10.1016/0092-8674(80)90128-2. [DOI] [PubMed] [Google Scholar]
  24. Pevsner J., Hsu S. C., Braun J. E., Calakos N., Ting A. E., Bennett M. K., Scheller R. H. Specificity and regulation of a synaptic vesicle docking complex. Neuron. 1994 Aug;13(2):353–361. doi: 10.1016/0896-6273(94)90352-2. [DOI] [PubMed] [Google Scholar]
  25. Pirrotta V. Vectors for P-mediated transformation in Drosophila. Biotechnology. 1988;10:437–456. doi: 10.1016/b978-0-409-90042-2.50028-3. [DOI] [PubMed] [Google Scholar]
  26. Salzberg A., D'Evelyn D., Schulze K. L., Lee J. K., Strumpf D., Tsai L., Bellen H. J. Mutations affecting the pattern of the PNS in Drosophila reveal novel aspects of neuronal development. Neuron. 1994 Aug;13(2):269–287. doi: 10.1016/0896-6273(94)90346-8. [DOI] [PubMed] [Google Scholar]
  27. Schiavo G., Benfenati F., Poulain B., Rossetto O., Polverino de Laureto P., DasGupta B. R., Montecucco C. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature. 1992 Oct 29;359(6398):832–835. doi: 10.1038/359832a0. [DOI] [PubMed] [Google Scholar]
  28. Schiavo G., Gmachl M. J., Stenbeck G., Söllner T. H., Rothman J. E. A possible docking and fusion particle for synaptic transmission. Nature. 1995 Dec 14;378(6558):733–736. doi: 10.1038/378733a0. [DOI] [PubMed] [Google Scholar]
  29. Schulze K. L., Littleton J. T., Salzberg A., Halachmi N., Stern M., Lev Z., Bellen H. J. rop, a Drosophila homolog of yeast Sec1 and vertebrate n-Sec1/Munc-18 proteins, is a negative regulator of neurotransmitter release in vivo. Neuron. 1994 Nov;13(5):1099–1108. doi: 10.1016/0896-6273(94)90048-5. [DOI] [PubMed] [Google Scholar]
  30. Sheng Z. H., Rettig J., Takahashi M., Catterall W. A. Identification of a syntaxin-binding site on N-type calcium channels. Neuron. 1994 Dec;13(6):1303–1313. doi: 10.1016/0896-6273(94)90417-0. [DOI] [PubMed] [Google Scholar]
  31. Sweeney S. T., Broadie K., Keane J., Niemann H., O'Kane C. J. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron. 1995 Feb;14(2):341–351. doi: 10.1016/0896-6273(95)90290-2. [DOI] [PubMed] [Google Scholar]
  32. Söllner T., Bennett M. K., Whiteheart S. W., Scheller R. H., Rothman J. E. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell. 1993 Nov 5;75(3):409–418. doi: 10.1016/0092-8674(93)90376-2. [DOI] [PubMed] [Google Scholar]
  33. 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 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  34. Tepass U., Theres C., Knust E. crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell. 1990 Jun 1;61(5):787–799. doi: 10.1016/0092-8674(90)90189-l. [DOI] [PubMed] [Google Scholar]
  35. Vactor D. V., Sink H., Fambrough D., Tsoo R., Goodman C. S. Genes that control neuromuscular specificity in Drosophila. Cell. 1993 Jun 18;73(6):1137–1153. doi: 10.1016/0092-8674(93)90643-5. [DOI] [PubMed] [Google Scholar]
  36. Vale R. D. Intracellular transport using microtubule-based motors. Annu Rev Cell Biol. 1987;3:347–378. doi: 10.1146/annurev.cb.03.110187.002023. [DOI] [PubMed] [Google Scholar]
  37. Xu T., Rubin G. M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development. 1993 Apr;117(4):1223–1237. doi: 10.1242/dev.117.4.1223. [DOI] [PubMed] [Google Scholar]
  38. Xue F., Cooley L. kelch encodes a component of intercellular bridges in Drosophila egg chambers. Cell. 1993 Mar 12;72(5):681–693. doi: 10.1016/0092-8674(93)90397-9. [DOI] [PubMed] [Google Scholar]

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