567
Views
15
CrossRef citations to date
0
Altmetric
Original Article

Three-dimensional imaging of Drosophila motor synapses reveals ultrastructural organizational patternsFootnote*

, , &
Pages 237-246 | Received 26 Sep 2016, Accepted 24 Oct 2016, Published online: 16 Dec 2016

References

  • Ackermann, F., Waites, C.L., & Garner, C.C. (2015). Presynaptic active zones in invertebrates and vertebrates. EMBO Reports, 16, 923–938. doi: https://doi.org/10.15252/embr.201540434.
  • Alabi, A.A., & Tsien, R.W. (2012). Synaptic vesicle pools and dynamics. Cold Spring Harbor Perspectives in Biology, 4, a013680. doi: https://doi.org/10.1101/cshperspect.a013680.
  • Bruckner, J.J., Zhan, H., & O'Connor-Giles, K.M. (2015). Advances in imaging ultrastructure yield new insights into presynaptic biology. Frontiers in Cellular Neuroscience, 9, 1–16. doi: https://doi.org/10.3389/fncel.2015.00196.
  • Bruckner, J.J., Zhan, H., Gratz, S.J., Rao, X., Zilberg, G., & O?Connor-Giles, K.M. (in press). Fife organizes synaptic vesicles and calcium channels for high-probability neurotransmitter release. Journal of Cell Biology.
  • Budnik, V., Koh, Y.H., Guan, B., Hartmann, B., Hough, C., Woods, D., & Gorczyca, M. (1996). Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron, 17, 627–640. doi: https://doi.org/10.1016/S0896-6273(00)80196-8.
  • Burette, A.C., Lesperance, T., Crum, J., Martone, M., Volkmann, N., Ellisman, M.H., & Weinberg, R.J. (2012). Electron tomographic analysis of synaptic ultrastructure. Journal of Comparative Neurology, 520, 2697–2711. doi: 10.1002/cne.23067.
  • Chen, X., Nelson, C.D., Li, X., Winters, C.A., Azzam, R., Sousa, A.A., …, Reese, T.S. (2011). PSD-95 is required to sustain the molecular organization of the postsynaptic density. Journal of Neuroscience, 31, 6329–6338. doi: 10.1523/JNEUROSCI.5968-10.2011.
  • Chen, X., Winters, C., Azzam, R., Li, X., Galbraith, J.A., Leapman, R.D., & Reese, T.S. (2008). Organization of the core structure of the postsynaptic density. Proceedings of the National Academy of Sciences of the USA, 105, 4453–4458. doi: 10.1073/pnas.0800897105.
  • Chen, X., Winters, C.A., & Reese, T.S. (2008). Life inside a thin section: tomography. Journal of Neuroscience, 28, 9321–9327. doi: 10.1523/JNEUROSCI.2992-08.2008.
  • Choquet, D., & Triller, A. (2013). The dynamic synapse. Neuron, 80, 691–703. doi: 10.1016/j.neuron.2013.10.013.
  • Daniels, R.W., Collins, C.A., Chen, K., Gelfand, M.V., Featherstone, D.E., & DiAntonio, A. (2006). A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle. Neuron, 49, 11–16. doi: 10.1016/j.neuron.2005.11.032.
  • De Robertis, E.D., & Bennett, H.S. (1955). Some features of the submicroscopic morphology of synapses in frog and earthworm. Journal of Biophysical and Biochemical Cytology, 1, 47–58. doi: 10.1083/jcb.1.1.47.
  • Denker, A., & Rizzoli, S.O. (2010). Synaptic vesicle pools: An update. Frontiers in Synaptic Neuroscience, 2, 135. doi:10.3389/fnsyn.2010.00135.
  • Eggermann, E., Bucurenciu, I., Goswami, S.P., & Jonas, P. (2012). Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses. Nature Reviews Neuroscience, 13, 7–21. doi: 10.1038/nrn3125
  • Feng, W., & Zhang, M. (2009). Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density. Nature Reviews Neuroscience, 10, 87–99. doi: 10.1038/nrn2540.
  • Fernández-Busnadiego, R., Asano, S., Oprisoreanu, A.M., Sakata, E., Doengi, M., Kochovski, Z., …, Lučić, V. (2013). Cryo-electron tomography reveals a critical role of RIM1α in synaptic vesicle tethering. Journal of Cell Biology, 201, 725–740. doi: 10.1083/jcb.201206063.
  • Fernández-Busnadiego, R., Schrod, N., Kochovski, Z., Asano, S., Vanhecke, D., Baumeister, W., & Lučić, V. (2011). Insights into the molecular organization of the neuron by cryo-electron tomography. Journal of Electron Microscopy, 60, S137–S148. doi: 10.1093/jmicro/dfr018.
  • Fernández-Busnadiego, R., Zuber, B., Maurer, U.E., Cyrklaff, M., Baumeister, W., & Lučić, V. (2010). Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography. Journal of Cell Biology, 188, 145–156. doi: 10.1083/jcb.200908082.
  • Fouquet, W., Owald, D., Wichmann, C., Mertel, S., Depner, H., Dyba, M., …, Sigrist, S.J. (2009). Maturation of active zone assembly by Drosophila Bruchpilot. Journal of Cell Biology, 186, 129–145. doi: 10.1083/jcb.200812150.
  • Gold, M.G. (2012). A frontier in the understanding of synaptic plasticity: solving the structure of the postsynaptic density. Bioessays, 34, 599–608. doi: 10.1002/bies.201200009.
  • Gracheva, E.O., Maryon, E.B., Berthelot-Grosjean, M., & Richmond, J.E. (2010). Differential regulation of synaptic vesicle tethering and docking by UNC-18 and TOM-1. Frontiers in Synaptic Neuroscience, 2, 141. doi: 10.3389/fnsyn.2010.00141.
  • Hammarlund, M., Palfreyman, M.T., Watanabe, S., Olsen, S., & Jorgensen, E.M. (2007). Open syntaxin docks synaptic vesicles. PLoS Biol, 5, e198. doi: 10.1371/journal.pbio.0050198.
  • Harlow, M.L., Ress, D., Stoschek, A., Marshall, R.M., & McMahan, U.J. (2001). The architecture of active zone material at the frog's neuromuscular junction. Nature, 409, 479–484. doi: 10.1038/35054000.
  • Helmprobst, F., Frank, M., & Stigloher, C. (2015). The presynaptic architecture of the larval zebrafish neuromuscular junction. Journal of Comparative Neurology, 523, 1984–1997. doi: 10.1002/cne.23775.
  • High, B., Cole, A.A., Chen, X., & Reese, T.S. (2015). Electron microscopic tomography reveals discrete transcleft elements at excitatory and inhibitory synapses. Frontiers in Synaptic Neuroscience, 7, 9. doi: 10.3389/fnsyn.2015.00009.
  • Hirokawa, N., Sobue, K., Kanda, K., Harada, A., & Yorifuji, H. (1989). The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1. Journal of Cell Biology, 108, 111–126. doi: 10.1083/jcb.108.1.111.
  • Ichimura, T., & Hashimoto, P.H. (1988). Structural components in the synaptic cleft captured by freeze-substitution and deep etching of directly frozen cerebellar cortex. Journal of Neurocytology, 17, 3–12. doi: 10.1007/BF01735373.
  • Imig, C., Min, S.W., Krinner, S., Arancillo, M., Rosenmund, C., Südhof, T.C., …, Cooper, B.H. (2014). The morphological and molecular nature of synaptic vesicle priming at presynaptic active zones. Neuron, 84, 416–431. doi: 10.1016/j.neuron.2014.10.009.
  • Jiao, W., Masich, S., Franzén, O., & Shupliakov, O. (2010). Two pools of vesicles associated with the presynaptic cytosolic projection in Drosophila neuromuscular junctions. Journal of Structural Biology, 172, 389–394. doi: 10.1016/j.jsb.2010.07.007.
  • Karunanithi, S., Marin, L., Wong, K., & Atwood, H.L. (2002). Quantal size and variation determined by vesicle size in normal and mutant Drosophila glutamatergic synapses. Journal of Neuroscience, 22, 10267–10276.
  • Kim, E., & Sheng, M. (2004). PDZ domain proteins of synapses. Nature Reviews Neuroscience, 5, 771–781. doi: 10.1038/nrn1517.
  • Koper, A., Schenck, A., & Prokop, A. (2012). Analysis of adhesion molecules and basement membrane contributions to synaptic adhesion at the Drosophila embryonic NMJ. PLoS ONE, 7, e36339. doi: 10.1371/journal.pone.0036339.
  • Korogod, N., Petersen, C.C.H., & Knott, G.W. (2015). Ultrastructural analysis of adult mouse neocortex comparing aldehyde perfusion with cryo fixation. Elife, 4, 241. doi: 10.7554/eLife.05793.
  • Kremer, J.R., Mastronarde, D.N., & McIntosh, J.R. (1996). Computer visualization of three-dimensional image data using IMOD. Journal of Structural Biology, 116, 71–76. doi: 10.1006/jsbi.1996.0013.
  • Landis, D.M., Hall, A.K., Weinstein, L.A., & Reese, T.S. (1988). The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse. Neuron, 1, 201–209. doi: 10.1016/0896-6273(88)90140-7.
  • Linsalata, A.E., Chen, X., Winters, C.A., & Reese, T.S. (2014). Electron tomography on γ-aminobutyric acid-ergic synapses reveals a discontinuous postsynaptic network of filaments. Journal of Comparative Neurology, 522, 921–936. doi: 10.1002/cne.23453.
  • Liu, K.S.Y., Siebert, M., Mertel, S., Knoche, E., Wegener, S., Wichmann, C., …, Sigrist, S.J. (2011). RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. Science, 334, 1565–1569. doi: 10.1038/ncomms12604.
  • Lučić, V., Yang, T., Schweikert, G., Förster, F., & Baumeister, W. (2005). Morphological characterization of molecular complexes present in the synaptic cleft. Structure, 13, 423–434. doi: 10.1016/j.str.2005.02.005.
  • Mastronarde, D.N. (2005). Automated electron microscope tomography using robust prediction of specimen movements. Journal of Structural Biology, 152, 36–51. doi: 10.1016/j.jsb.2005.07.007.
  • Matkovic, T., Siebert, M., Knoche, E., Depner, H., Mertel, S., Owald, D., …, Sigrist, S.J. (2013). The Bruchpilot cytomatrix determines the size of the readily releasable pool of synaptic vesicles. Journal of Cell Biology, 202, 667–683. doi: 10.1523/JNEUROSCI.6698-10.2011.
  • McDonald, K.L., Sharp, D.J., & Rickoll, W. (2012). Transmission electron microscopy of thin sections of Drosophila: High-pressure freezing and freeze-substitution. Cold Spring Harbor Protocols, 2012, 510–515. doi: 10.1101/pdb.prot068403.
  • Nagwaney, S., Harlow, M.L., Jung, J.H., Szule, J.A., Ress, D., Xu, J., …, McMahan, U.J. (2009). Macromolecular connections of active zone material to docked synaptic vesicles and presynaptic membrane at neuromuscular junctions of mouse. Journal of Comparative Neurology, 513, 457–468. doi: 10.1002/cne.21975.
  • Palay, S.L., & Palade, G.E. (1955). The fine structure of neurons. Journal of Biophysical and Biochemical Cytology, 1, 69–88. doi: 10.1083/jcb.1.1.69.
  • Perez de Arce, K., Schrod, N., Metzbower, S.W.R., Allgeyer, E., Kong, G.K.W., Tang, A.H., …, Biederer, T. (2015). Topographic mapping of the synaptic cleft into adhesive nanodomains. Neuron, 88, 1165–1172. doi: 10.1016/j.neuron.2015.11.011.
  • Prokop, A. (1999). Integrating bits and pieces: synapse structure and formation in Drosophila embryos. Cell and Tissue Research, 297, 169–186. doi: 10.1007/s004410051345.
  • R Core Team. (2016). R 3.3.1: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
  • Rizzoli, S.O., & Betz, W.J. (2005). Synaptic vesicle pools. Nature Reviews Neuroscience, 6, 57–69. doi: 10.1038/nrn1583.
  • Rostaing, P., Real, E., Siksou, L., Lechaire, J.P., Boudier, T., Boeckers, T.M., …, Marty, S. (2006). Analysis of synaptic ultrastructure without fixative using high-pressure freezing and tomography. European Journal of Neuroscience, 24, 3463–3474. doi: 10.1111/j.1460-9568.2006.05234.x.
  • Rostaing, P., Weimer, R.M., Jorgensen, E.M., Triller, A., & Bessereau, J.L. (2004). Preservation of immunoreactivity and fine structure of adult C. elegans tissues using high-pressure freezing. Journal of Histochemistry and Cytochemistry, 52, 1–12. doi: 10.1177/002215540405200101.
  • Sheng, M., & Hoogenraad, C.C. (2007). The postsynaptic architecture of excitatory synapses: a more quantitative view. Annual Review of Biochemistry, 76, 823–847. doi: 10.1146/annurev.biochem.76.060805.160029.
  • Shtrahman, M., Yeung, C., Nauen, D.W., Bi, G.Q., & Wu, X.L. (2005). Probing vesicle dynamics in single hippocampal synapses. Biophysical Journal, 89, 3615–3627. doi: 10.1529/biophysj.105.059295.
  • Siksou, L., Rostaing, P., Lechaire, J.P., Boudier, T., Ohtsuka, T., Fejtová, A., …, Marty, S. (2007). Three-dimensional architecture of presynaptic terminal cytomatrix. Journal of Neuroscience, 27, 6868–6877. doi: 10.1523/JNEUROSCI.1773-07.2007.
  • Siksou, L., Triller, A., & Marty, S. (2011). Ultrastructural organization of presynaptic terminals. Current Opinion in Neurobiology, 21, 261–268. doi: 10.1016/j.conb.2010.12.003.
  • Siksou, L., Varoqueaux, F., Pascual, O., Triller, A., Brose, N., & Marty, S. (2009). A common molecular basis for membrane docking and functional priming of synaptic vesicles. European Journal of Neuroscience, 30, 49–56. doi: 10.1111/j.1460-9568.2009.06811.x.
  • Stigloher, C., Zhan, H., Zhen, M., Richmond, J., & Bessereau, J.L. (2011). The presynaptic dense projection of the Caenorhabditis elegans cholinergic neuromuscular junction localizes synaptic vesicles at the active zone through SYD-2/liprin and UNC-10/RIM-dependent interactions. Journal of Neuroscience, 31, 4388–4396. doi: 10.1523/JNEUROSCI.6164-10.2011.
  • Szule, J.A., Jung, J.H., & McMahan, U.J. (2015). The structure and function of “active zone material” at synapses. Philosophical Transactions of the Royal Society B: Biological Sciences, 370, 20140189. doi:10.1098/rstb.2014.0189.
  • Tang, A.H., Chen, H., Li, T.P., Metzbower, S.R., MacGillavry, H.D., & Blanpied, T.A. (2016). A trans-synaptic nanocolumn aligns neurotransmitter release to receptors. Nature, 536, 210–214. doi:10.1038/nature19058.
  • Torrealba, F., & Carrasco, M.A. (2004). A review on electron microscopy and neurotransmitter systems. Brain Research Reviews, 47, 5–17. doi: 10.1016/j.brainresrev.2004.06.004.
  • Weimer, R.M., Gracheva, E.O., Meyrignac, O., Miller, K.G., Richmond, J.E., & Bessereau, J.L. (2006). UNC-13 and UNC-10/rim localize synaptic vesicles to specific membrane domains. Journal of Neuroscience, 26, 8040–8047. doi: 10.1523/JNEUROSCI.2350-06.2006.
  • Wickham, H. (2009). ggplot2: Elegant graphics for data analysis. New York: Springer-Verlag. doi: 10.1007/978-0-387-98141-3.
  • Zuber, B., Nikonenko, I., Klauser, P., Muller, D., & Dubochet, J. (2005). The mammalian central nervous synaptic cleft contains a high density of periodically organized complexes. Proceedings of National Academy Sciences USA, 102, 19192–19197. doi: 10.1073/pnas.0509527102.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.