Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse - PubMed (original) (raw)
. 1993 Aug;118(4):1077-88.
doi: 10.1242/dev.118.4.1077.
Affiliations
- PMID: 8269841
- DOI: 10.1242/dev.118.4.1077
Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse
J T Littleton et al. Development. 1993 Aug.
Abstract
Synaptotagmin is a synaptic vesicle-specific integral membrane protein that has been suggested to play a key role in synaptic vesicle docking and fusion. By monitoring Synaptotagmin's cellular and subcellular distribution during development, it is possible to study synaptic vesicle localization and transport, and synapse formation. We have initiated the study of Synaptotagmin's expression during Drosophila neurogenesis in order to follow synaptic vesicle movement prior to and during synapse formation, as well as to localize synaptic sites in Drosophila. In situ hybridizations to whole-mount embryos show that synaptotagmin (syt) message is present in the cell bodies of all peripheral nervous system neurons and many, if not all, central nervous system neurons during neurite outgrowth and synapse formation, and in mature neurons. Immunocytochemical staining with antisera specific to Synaptotagmin indicates that the protein is present at all stages of the Drosophila life cycle following germ band retraction. In embryos, Synaptotagmin is only transiently localized to the cell body of neurons and is transported rapidly along axons during axonogenesis. After synapse formation, Synaptotagmin accumulates in a punctate pattern at all identifiable synaptic contact sites, suggesting a general role for Synaptotagmin in synapse function. In embryos and larvae, the most intense staining is found along two broad longitudinal tracts on the dorsal side of the ventral nerve cord and the brain, and at neuromuscular junctions in the periphery. In the adult head, Synaptotagmin localizes the discrete regions of the neurophil where synapses are predicted to occur. These data indicate that synaptic vesicles are present in axons before synapse formation, and become restricted to synaptic contact sites after synapses are formed. Since a similar expression pattern of Synaptotagmin has been reported in mammals, we propose that the function of Synaptotagmin and the mechanisms governing localization of the synaptic vesicle before and after synapse formation are conserved in invertebrate and vertebrate species. The ability to mark synapses in Drosophila should facilitate the study of synapse formation and function, providing a new tool to dissect the molecular mechanisms underlying these processes.
Similar articles
- Roles of SNARE proteins and synaptotagmin I in synaptic transmission: studies at the Drosophila neuromuscular synapse.
Kidokoro Y. Kidokoro Y. Neurosignals. 2003 Jan-Feb;12(1):13-30. doi: 10.1159/000068912. Neurosignals. 2003. PMID: 12624525 Review. - Morphologically docked synaptic vesicles are reduced in synaptotagmin mutants of Drosophila.
Reist NE, Buchanan J, Li J, DiAntonio A, Buxton EM, Schwarz TL. Reist NE, et al. J Neurosci. 1998 Oct 1;18(19):7662-73. doi: 10.1523/JNEUROSCI.18-19-07662.1998. J Neurosci. 1998. PMID: 9742137 Free PMC article. - Immunocytochemical analysis of axonal outgrowth in synaptotagmin mutations.
Littleton JT, Upton L, Kania A. Littleton JT, et al. J Neurochem. 1995 Jul;65(1):32-40. doi: 10.1046/j.1471-4159.1995.65010032.x. J Neurochem. 1995. PMID: 7790877 - The effect on synaptic physiology of synaptotagmin mutations in Drosophila.
DiAntonio A, Schwarz TL. DiAntonio A, et al. Neuron. 1994 Apr;12(4):909-20. doi: 10.1016/0896-6273(94)90342-5. Neuron. 1994. PMID: 7909234 - Synaptotagmin controls and modulates synaptic-vesicle fusion in a Ca(2+)-dependent manner.
Littleton JT, Bellen HJ. Littleton JT, et al. Trends Neurosci. 1995 Apr;18(4):177-83. doi: 10.1016/0166-2236(95)93898-8. Trends Neurosci. 1995. PMID: 7778189 Review.
Cited by
- Differential regulation of evoked and spontaneous neurotransmitter release by C-terminal modifications of complexin.
Buhl LK, Jorquera RA, Akbergenova Y, Huntwork-Rodriguez S, Volfson D, Littleton JT. Buhl LK, et al. Mol Cell Neurosci. 2013 Jan;52:161-72. doi: 10.1016/j.mcn.2012.11.009. Epub 2012 Nov 16. Mol Cell Neurosci. 2013. PMID: 23159779 Free PMC article. - Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport.
Martin M, Iyadurai SJ, Gassman A, Gindhart JG Jr, Hays TS, Saxton WM. Martin M, et al. Mol Biol Cell. 1999 Nov;10(11):3717-28. doi: 10.1091/mbc.10.11.3717. Mol Biol Cell. 1999. PMID: 10564267 Free PMC article. - Gap junction proteins expressed during development are required for adult neural function in the Drosophila optic lamina.
Curtin KD, Zhang Z, Wyman RJ. Curtin KD, et al. J Neurosci. 2002 Aug 15;22(16):7088-96. doi: 10.1523/JNEUROSCI.22-16-07088.2002. J Neurosci. 2002. PMID: 12177205 Free PMC article. - Characterization of a yeast interfering RNA larvicide with a target site conserved in the synaptotagmin gene of multiple disease vector mosquitoes.
Mysore K, Li P, Wang CW, Hapairai LK, Scheel ND, Realey JS, Sun L, Roethele JB, Severson DW, Wei N, Duman-Scheel M. Mysore K, et al. PLoS Negl Trop Dis. 2019 May 20;13(5):e0007422. doi: 10.1371/journal.pntd.0007422. eCollection 2019 May. PLoS Negl Trop Dis. 2019. PMID: 31107878 Free PMC article. - Modeling spinal muscular atrophy in Drosophila.
Chang HC, Dimlich DN, Yokokura T, Mukherjee A, Kankel MW, Sen A, Sridhar V, Fulga TA, Hart AC, Van Vactor D, Artavanis-Tsakonas S. Chang HC, et al. PLoS One. 2008 Sep 15;3(9):e3209. doi: 10.1371/journal.pone.0003209. PLoS One. 2008. PMID: 18791638 Free PMC article.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Molecular Biology Databases
Miscellaneous