Colocalization of different neurotransmitter transporters on synaptic vesicles is sparse except for VGLUT1 and ZnT3
Open accessAbstract
Vesicular transporters (VTs) define the type of neurotransmitter that synaptic vesicles (SVs) store and release. While certain mammalian neurons release multiple transmitters, it is not clear whether the release occurs from the same or distinct vesicle pools at the synapse. Using quantitative single-vesicle imaging, we show that a vast majority of SVs in the rodent brain contain only one type of VT, indicating specificity for a single neurotransmitter. Interestingly, SVs containing dual transporters are highly diverse (27 types) but small in proportion (2% of all SVs), excluding the largest pool that carries VGLUT1 and ZnT3 (34%). Using VGLUT1-ZnT3 SVs, we demonstrate that the transporter colocalization influences the SV content and synaptic quantal size. Thus, the presence of diverse transporters on the same vesicle is bona fide, and depending on the VT types, this may act to regulate neurotransmitter type, content, and release in space and time.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Complementary dependencies may explain observed synergies between vGluT and VAChT or vGluT and ZnT3 on the same synaptic vesicle.
“These complementary dependencies may explain the observed synergies between vGluT and VAChT or vGluT and the vesicular zinc transporter (ZnT3) when these are localized to the same synaptic vesicle.5,21,22”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [5]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
NIH Image to ImageJ: 25 years of image analysis
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012) · Nature Methods · doi:10.1038/nmeth.2089 · Cited by 64,638 · see citing works
UniProt: a worldwide hub of protein knowledge
The UniProt Consortium (2019) · Nucleic Acids Research · doi:10.1093/nar/gky1049 · Cited by 7,698 · see citing works
Global quantification of mammalian gene expression control
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566 · see citing works
Pérez-Riverol, Y., Csordas, A., Bai, J.-W., Bernal-Llinares, M., Hewapathirana, S., Kundu, D. J., Inuganti, A., Griss, J., Mayer, G., Eisenacher, M., et al. (2018) · Nucleic Acids Res. · doi:10.1093/nar/gky1106 · Cited by 6,216 · see citing works
Molecular Architecture of the Mouse Nervous System
Zeisel, A., Hochgerner, H., Lönnerberg, P., Johnsson, A., Memic, F., van der Zwan, J., Häring, M., Braun, E., Borm, L. E., La Manno, G., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.021 · Cited by 2,995 · see citing works
Schägger, H. (2006) · Nature Protocols · doi:10.1038/nprot.2006.4 · Cited by 2,519 · see citing works
Molecular anatomy of a trafficking organelle
Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., et al. (2006) · Cell · doi:10.1016/j.cell.2006.10.030 · Cited by 2,373 · see citing works
Self-citationSingle-pot, solid-phase-enhanced sample preparation for proteomics experiments
Hughes, C. S., Moggridge, S., Müller, T., Sorensen, P. H. B., Morin, G. B., & Krijgsveld, J. (2018) · Nature Protocols · doi:10.1038/s41596-018-0082-x · Cited by 1,938 · see citing works
The neurobiology of zinc in health and disease
Frederickson, C. J., Koh, J., & Bush, A. I. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1671 · Cited by 1,841 · see citing works
Kaech, S., & Banker, G. A. (2006) · Nature Protocols · doi:10.1038/nprot.2006.356 · Cited by 1,705 · see citing works
Ovesný, M., Křížek, P., Borkovec, J., Švindrych, Z., & Hagen, G. M. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu202 · Cited by 1,515 · see citing works
Bruderer, R., Bernhardt, O. M., Gandhi, T., Miladinović, S. M., Cheng, L.-Y., Messner, S., Ehrenberger, T., Zanotelli, V., Butscheid, Y., Escher, C., et al. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m114.044305 · Cited by 1,238 · see citing works
Huttner, W. Β., SCHIEBLER, W., Greengard, P., & Camilli, P. V. D. (1983) · The Journal of Cell Biology · doi:10.1083/jcb.96.5.1374 · Cited by 1,172 · see citing works
Super-resolution microscopy with DNA-PAINT
Schnitzbauer, J., Strauss, M. T., Schlichthaerle, T., Schueder, F., & Jungmann, R. (2017) · Nature Protocols · doi:10.1038/nprot.2017.024 · Cited by 1,047 · see citing works
An optimized fluorescent probe for visualizing glutamate neurotransmission
Marvin, J. S., Borghuis, B. G., Tian, L., Cichon, J., Harnett, M. T., Akerboom, J., Gordus, A. G., Renninger, S. L., Chen, T., Bargmann, C. I., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2333 · Cited by 1,006 · see citing works
A 38,000-dalton membrane protein (p38) present in synaptic vesicles.
Jahn, R., SCHIEBLER, W., Ouimet, C. C., & Greengard, P. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.12.4137 · Cited by 851 · see citing works
Self-citationComposition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins
Wilhelm, B. G., Mandad, S., Truckenbrodt, S., Kröhnert, K., Schäfer, C., Rammner, B., Koo, S. J., Claßen, G. A., Krauss, M., Haucke, V., et al. (2014) · Science · doi:10.1126/science.1252884 · Cited by 770 · see citing works
Self-citationDopaminergic neurons inhibit striatal output through non-canonical release of GABA
Tritsch, N. X., Ding, J. B., & Sabatini, B. L. (2012) · Nature · doi:10.1038/nature11466 · Cited by 576 · see citing works
Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene.
Cole, T., Wenzel, H., Kafer, K. E., Schwartzkroin, P., & Palmiter, R. (1999) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.96.4.1716 · Cited by 560 · see citing works
Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate
Stuber, G. D., Hnasko, T. S., Britt, J. P., Edwards, R. H., & Bonci, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1754-10.2010 · Cited by 529 · see citing works
SR-Tesseler: a method to segment and quantify localization-based super-resolution microscopy data
Levet, F., Hosy, E., Kechkar, A., Butler, C., Beghin, A., Choquet, D., & Sibarita, J.-B. (2015) · Nature Methods · doi:10.1038/nmeth.3579 · Cited by 502 · see citing works
Takamori, S., Rhee, J. S., Rosenmund, C., & Jahn, R. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-22-j0002.2001 · Cited by 492 · see citing works
Self-citationGenetically encoded FRET sensors to monitor intracellular Zn2+ homeostasis
Vinkenborg, J. L., Nicolson, T. J., Bellomo, E. A., Koay, M. S. T., Rutter, G. A., & Merkx, M. (2009) · Nature Methods · doi:10.1038/nmeth.1368 · Cited by 426 · see citing works
Stability, affinity, and chromatic variants of the glutamate sensor iGluSnFR
Marvin, J. S., Scholl, B., Wilson, D. E., Podgorski, K., Kazemipour, A., Müller, J. A., Schoch, S., Quiroz, F. J. U., Rebola, N., Bao, H., et al. (2018) · Nature Methods · doi:10.1038/s41592-018-0171-3 · Cited by 412 · see citing works
Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo
Hnasko, T. S., Chuhma, N., Zhang, H., Goh, G. Y., Sulzer, D., Palmiter, R. D., Rayport, S., & Edwards, R. H. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.012 · Cited by 405 · see citing works
Detection of spontaneous synaptic events with an optimally scaled template
Clements, J. D., & Bekkers, J. M. (1997) · Biophysical Journal · doi:10.1016/s0006-3495(97)78062-7 · Cited by 401 · see citing works
From glutamate co-release to vesicular synergy: vesicular glutamate transporters
El Mestikawy, S., Wallén-Mackenzie, Å., Fortin, G. M., Descarries, L., & Trudeau, L.-E. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2969 · Cited by 385 · see citing works
GABA/glutamate co-release controls habenula output and is modified by antidepressant treatment
Shabel, S. J., Proulx, C. D., Piriz, J., & Malinow, R. (2014) · Science · doi:10.1126/science.1250469 · Cited by 369 · see citing works
Single rodent mesohabenular axons release glutamate and GABA
Root, D. H., Mejias-Aponte, C. A., Zhang, S., Wang, H.-L., Hoffman, A. F., Lupica, C. R., & Morales, M. (2014) · Nature Neuroscience · doi:10.1038/nn.3823 · Cited by 349 · see citing works
Ren, J., Qin, C., Hu, F., Tan, J., Qiu, L., Zhao, S., Feng, G., & Luo, M. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.038 · Cited by 315 · see citing works
Qin, Y., Dittmer, P. J., Park, J. G., Jansen, K. B., & Palmer, A. E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015686108 · Cited by 307 · see citing works
Neurotransmitter Corelease: Mechanism and Physiological Role
Hnasko, T. S., & Edwards, R. H. (2012) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020911-153315 · Cited by 284 · cited 1× · see citing works
“Corelease of multiple neurotransmitters from the same vesicle Release of multiple neurotransmitters from the same neuron or synapse is well documented (El Mestikawy et al., 2011; Granger et al., 2017; Hnasko and Edwards, 2012).”
BackgroundMechanisms and functions of GABA co-release
Tritsch, N. X., Granger, A. J., & Sabatini, B. L. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2015.21 · Cited by 261 · see citing works
Fast synaptic subcortical control of hippocampal circuits
Varga, V., Losonczy, A., Zemelman, B. V., Borhegyi, Z., Nyiri, G., Domonkos, A., Hangya, B., Holderith, N., Magee, J. C., & Freund, T. F. (2009) · Science · doi:10.1126/science.1178307 · Cited by 248 · see citing works
Chuhma, N., Mingote, S., Moore, H., & Rayport, S. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.027 · Cited by 233 · see citing works
Dual-transmitter neurons: functional implications of co-release and co-transmission
Vaaga, C. E., Borisovska, M., & Westbrook, G. L. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.04.010 · Cited by 221 · see citing works
Zinc Dynamics and Action at Excitatory Synapses
Vergnano, A. M., Rebola, N., Savtchenko, L. P., Pinheiro, P. S., Casado, M., Kieffer, B. L., Rusakov, D. A., Mulle, C., & Paoletti, P. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.034 · Cited by 213 · see citing works
The vesicular glutamate transporter VGLUT3 synergizes striatal acetylcholine tone
Gras, C., Amilhon, B., Lepicard, È. M., Poirel, O., Vinatier, J., Herbin, M., Dumas, S., Tzavara, E. T., Wade, M. R., Nomikos, G. G., et al. (2008) · Nature Neuroscience · doi:10.1038/nn2052 · Cited by 211 · see citing works
Corelease of acetylcholine and GABA from cholinergic forebrain neurons
Saunders, A., Granger, A. J., & Sabatini, B. L. (2015) · eLife · doi:10.7554/elife.06412 · Cited by 200 · see citing works
Binding to nanopatterned antigens is dominated by the spatial tolerance of antibodies
SHAW, A. R., Hoffecker, I. T., Smyrlaki, I., Rosa, J., Grevys, A., Bratlie, D. B., Sandlie, I., Michaelsen, T. E., Andersen, J. T., & Högberg, B. (2019) · Nature Nanotechnology · doi:10.1038/s41565-018-0336-3 · Cited by 196 · see citing works
Grønborg, M., Pavlos, N. J., Brunk, I., Chua, J. J. E., Münster‐Wandowski, A., Riedel, D., Ahnert‐Hilger, G., Urlaub, H., & Jahn, R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4074-09.2010 · Cited by 194 · see citing works
Self-citationCoordinate-based colocalization analysis of single-molecule localization microscopy data
Malkusch, S., Endesfelder, U., Mondry, J., Gelléri, M., Verveer, P. J., & Heilemann, M. (2011) · Histochemistry and Cell Biology · doi:10.1007/s00418-011-0880-5 · Cited by 189 · see citing works
Mutch, S. A., Kensel-Hammes, P., Gadd, J. C., Fujimoto, B. S., Allen, R. W., Schiro, P. G., Lorenz, R. M., Kuyper, C. L., Kuo, J. S., Bajjalieh, S. M., et al. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3805-10.2011 · Cited by 185 · see citing works
Takamori, S., Riedel, D., & Jahn, R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-13-04904.2000 · Cited by 177 · see citing works
Self-citationCholinergic interneurons mediate fast VGluT3-dependent glutamatergic transmission in the striatum
Higley, M. J., Gittis, A. H., Oldenburg, I. A., Balthasar, N., Seal, R. P., Edwards, R. H., Lowell, B. B., Kreitzer, A. C., & Sabatini, B. L. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019155 · Cited by 175 · see citing works
Zinc transporter 3 (ZnT3) and vesicular zinc in central nervous system function
McAllister, B. B., & Dyck, R. H. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.06.006 · Cited by 170 · see citing works
Co-transmission of acetylcholine and GABA regulates hippocampal states
Takács, V. T., Cserép, C., Schlingloff, D., Pósfai, B., Szőnyi, A., Sos, K. E., Környei, Z., Dénes, Á., Gulyás, A. I., Freund, T. F., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05136-1 · Cited by 169 · see citing works
Adaptive-illumination STED nanoscopy
Heine, J., Reuss, M., Harke, B., D’Este, E., Sahl, S. J., & Hell, S. W. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1708304114 · Cited by 165 · see citing works
Self-citationMINSTED fluorescence localization and nanoscopy
Weber, M., Leutenegger, M., Stoldt, S., Jakobs, S., Mihaila, T. S., Butkevich, A. N., & Hell, S. W. (2021) · Nature Photonics · doi:10.1038/s41566-021-00774-2 · Cited by 156 · see citing works
Self-citationSynaptic and Vesicular Coexistence of VGLUT and VGAT in Selected Excitatory and Inhibitory Synapses
Zander, J.-F., Münster‐Wandowski, A., Brunk, I., Pahner, I., Gómez‐Lira, G., Heinemann, U., Gutiérrez, R., Laube, G., & Ahnert‐Hilger, G. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0141-10.2010 · Cited by 154 · see citing works
Root, D. H., Zhang, S., Barker, D. J., Miranda-Barrientos, J., Liu, B., Wang, H.-L., & Morales, M. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.063 · Cited by 153 · see citing works
Herzog, É., Takamori, S., Jahn, R., Brose, N., & Wojcik, S. M. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04144.x · Cited by 136 · see citing works
Self-citationControl of amygdala circuits by 5-HT neurons via 5-HT and glutamate cotransmission
Sengupta, A., Bocchio, M., Bannerman, D. M., Sharp, T., & Capogna, M. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2238-16.2016 · Cited by 136 · cited 1× · see citing works
“, 2010), or with serotonin in the hippocampal raphe nuclei projections (Sengupta et al., 2017; Varga et al., 2009), or with acetylcholine in striatal interneurons and medial habenula projections (Frahm et al.”
BackgroundSynaptic Vesicle Recycling Pathway Determines Neurotransmitter Content and Release Properties
Silm, K., Yang, J., Marcott, P. F., Asensio, C. S., Eriksen, J., Guthrie, D. A., Newman, A. H., Ford, C., & Edwards, R. H. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.031 · Cited by 131 · see citing works
AMPA receptor inhibition by synaptically released zinc
Kalappa, B. I., Anderson, C. T., Goldberg, J. M., Lippard, S. J., & Tzounopoulos, T. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1512296112 · Cited by 130 · see citing works
Liu, S., Plachez, C., Shao, Z., Puché, A. C., & Shipley, M. T. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3607-12.2013 · Cited by 124 · see citing works
Strong signal increase in STED fluorescence microscopy by imaging regions of subdiffraction extent
Göttfert, F., Pleiner, T., Heine, J., Westphal, V., Görlich, D., Sahl, S. J., & Hell, S. W. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1621495114 · Cited by 115 · see citing works
Self-citationHidden proteome of synaptic vesicles in the mammalian brain
Taoufiq, Z., Ninov, M., Villar‐Briones, A., Wang, H.-Y., Sasaki, T., Roy, M. C., Beauchain, F., Mori, Y., Yoshida, T., Takamori, S., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2011870117 · Cited by 105 · see citing works
Self-citationCircumvention of common labelling artefacts using secondary nanobodies
Sograte‐Idrissi, S., Schlichthaerle, T., Duque-Afonso, C. J., Alevra, M., Strauss, S., Moser, T., Jungmann, R., Rizzoli, S. O., & Opazo, F. (2020) · Nanoscale · doi:10.1039/d0nr00227e · Cited by 100 · see citing works
An essential role of acetylcholine-glutamate synergy at habenular synapses in nicotine dependence
Frahm, S., Antolin-Fontes, B., Görlich, A., Zander, J.-F., Ahnert-Hilger, G., & Ibañez-Tallon, I. (2015) · eLife · doi:10.7554/elife.11396 · Cited by 98 · see citing works
Farsi, Z., Preobraschenski, J., van den Bogaart, G., Riedel, D., Jahn, R., & Woehler, A. (2016) · Science · doi:10.1126/science.aad8142 · Cited by 96 · see citing works
Self-citationVglut1 and ZnT3 co-targeting mechanisms regulate vesicular zinc stores in PC12 cells
Salazar, G., Craige, B., Love, R., Kalman, D., & Faúndez, V. (2005) · Journal of Cell Science · doi:10.1242/jcs.02319 · Cited by 95 · see citing works
Multi-transmitter neurons in the mammalian central nervous system
Granger, A. J., Wallace, M. L., & Sabatini, B. L. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.04.007 · Cited by 95 · see citing works
Preobraschenski, J., Zander, J.-F., Suzuki, T., Ahnert‐Hilger, G., & Jahn, R. (2014) · Neuron · doi:10.1016/j.neuron.2014.11.008 · Cited by 87 · see citing works
Self-citationTrudeau, L., & Mestikawy, S. E. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00113 · Cited by 79 · see citing works
Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket Cells
Fasano, C., Rocchetti, J., Pietrajtis, K., Zander, J.-F., Manseau, F., Sakae, D. Y., Marcus-Sells, M., Ramet, L., Morel, L. J., Carrel, D., et al. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00140 · Cited by 63 · see citing works
Molecular and functional architecture of striatal dopamine release sites
Banerjee, A., Imig, C., Balakrishnan, K., Kershberg, L., Lipstein, N., Uronen, R.-L., Wang, J., Cai, X., Benseler, F., Rhee, J. S., et al. (2022) · Neuron · doi:10.1016/j.neuron.2021.10.028 · Cited by 58 · see citing works
Trist, B. G., Hare, D. J., & Double, K. L. (2018) · Cell chemical biology · doi:10.1016/j.chembiol.2018.05.004 · Cited by 50 · see citing works
Intracellular Zn2+ transients modulate global gene expression in dissociated rat hippocampal neurons
Sanford, L., Carpenter, M. C., & Palmer, A. E. (2019) · Scientific Reports · doi:10.1038/s41598-019-45844-2 · Cited by 49 · see citing works
Sub-nanomolar sensitive GZnP3 reveals TRPML1-mediated neuronal Zn2+ signals
Minckley, T. F., Zhang, C., Fudge, D. H., Dischler, A. M., LeJeune, K. D., Xu, H., & Qin, Y. (2019) · Nature Communications · doi:10.1038/s41467-019-12761-x · Cited by 46 · see citing works
Lavoie, N., Jeyaraju, D. V., Peralta, M. R., Seress, L., Pellegrini, L., & Tóth, K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4164-11.2011 · Cited by 42 · see citing works
Rapid purification and metabolomic profiling of synaptic vesicles from mammalian brain
Chantranupong, L., Saulnier, J. L., Wang, W., Jones, D. R., Pacold, M. E., & Sabatini, B. L. (2020) · eLife · doi:10.7554/elife.59699 · Cited by 41 · see citing works
Zimmermann, J., Herman, M. A., & Rosenmund, C. (2015) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2015.00016 · Cited by 37 · see citing works
Isolation of large dense-core vesicles from bovine adrenal medulla for functional studies
Birinci, Y., Preobraschenski, J., Ganzella, M., Jahn, R., & Park, Y. (2020) · Scientific Reports · doi:10.1038/s41598-020-64486-3 · Cited by 33 · see citing works
Self-citationSNARE Function Is Not Involved in Early Endosome Docking
Geumann, U., Barysch, S. V., Hoopmann, P., Jahn, R., & Rizzoli, S. O. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-05-0457 · Cited by 31 · see citing works
Self-citationAmyloids: Regulators of Metal Homeostasis in the Synapse
Kawahara, M., Kato‐Negishi, M., & Tanaka, K. (2020) · Molecules · doi:10.3390/molecules25061441 · Cited by 31 · see citing works
Goch, W., & Bal, W. (2020) · The Journal of Physical Chemistry A · doi:10.1021/acs.jpca.9b09441 · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Chen, B., Yu, P., Chan, W. N., Xie, F., Zhang, Y., Liang, L., Leung, K. T., Lo, K. W., Yu, J., Tse, G. M. K., et al. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01679-y · Cited by 420 · see citing works
Basal forebrain cholinergic signalling: development, connectivity and roles in cognition
Ananth, M. R., Rajebhosale, P., Kim, R., Talmage, D. A., & Role, L. W. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00677-x · Cited by 148 · see citing works
The proteomic landscape of synaptic diversity across brain regions and cell types
van Oostrum, M., Blok, T. M., Giandomenico, S. L., tom Dieck, S., Tushev, G., Fürst, N., Langer, J. D., & Schuman, E. M. (2023) · Cell · doi:10.1016/j.cell.2023.09.028 · Cited by 135 · see citing works
MINSTED nanoscopy enters the Ångström localization range
Weber, M., von der Emde, H., Leutenegger, M., Gunkel, P., Sambandan, S., Khan, T. A., Keller-Findeisen, J., Cordes, V. C., & Hell, S. W. (2023) · Nature Biotechnology · doi:10.1038/s41587-022-01519-4 · Cited by 94 · see citing works
Self-citationRelevance of interactions between dopamine and glutamate neurotransmission in schizophrenia
Buck, S. A., Erickson-Oberg, M. Q., Logan, R. W., & Freyberg, Z. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01649-w · Cited by 92 · see citing works
Mechanisms of NMDA receptor regulation
Mony, L., & Paoletti, P. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102815 · Cited by 71 · see citing works
Zinc in Cognitive Impairment and Aging
Sun, R., Wang, J., Feng, J., & Cao, B. (2022) · Biomolecules · doi:10.3390/biom12071000 · Cited by 61 · see citing works
Synaptic and circuit functions of multitransmitter neurons in the mammalian brain
Wallace, M. L., & Sabatini, B. L. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.003 · Cited by 59 · see citing works
Understanding the molecular diversity of synapses
van Oostrum, M., & Schuman, E. M. (2025) · Nature Reviews Neuroscience · doi:10.1038/s41583-024-00888-w · Cited by 49 · see citing works
From zinc homeostasis to disease progression: Unveiling the neurodegenerative puzzle
Fan, Y., Wu, T.-Y., Zhao, L., Jia, R., Hang, R., Hou, W., & Wang, Z. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2023.107039 · Cited by 47 · see citing works
Regulation of the mammalian-brain V-ATPase through ultraslow mode-switching
Kosmidis, E., Shuttle, C. G., Preobraschenski, J., Ganzella, M., Johnson, P. J., Veshaguri, S., Holmkvist, J., Møller, M. P., Marantos, O., Marcoline, F. V., et al. (2022) · Nature · doi:10.1038/s41586-022-05472-9 · Cited by 38 · see citing works
Self-citationAstrocytes release ATP/ADP and glutamate in flashes via vesicular exocytosis
Li, H., Zhao, Y., Dai, R., Geng, P., Weng, D., Wu, W., Yu, F., Lin, R., Wu, Z., Li, Y., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02851-8 · Cited by 40 · see citing works
A genetically encoded far-red fluorescent indicator for imaging synaptically released Zn 2+
Wu, T., Kumar, M., Zhang, J., Zhao, S., Drobizhev, M. A., McCollum, M., Anderson, C. T., Wang, Y., Pokorny, A., Tian, X., et al. (2023) · Science Advances · doi:10.1126/sciadv.add2058 · Cited by 33 · see citing works
ATG9 resides on a unique population of small vesicles in presynaptic nerve terminals
Binotti, B., Ninov, M., Cepeda, A. P., Ganzella, M., Matti, U., Riedel, D., Urlaub, H., Sambandan, S., & Jahn, R. (2023) · Autophagy · doi:10.1080/15548627.2023.2274204 · Cited by 30 · see citing works
Self-citationMolecular architecture of synaptic vesicles
Kravčenko, U., Ruwolt, M., Kroll, J., Yushkevich, A., Zenkner, M., Ruta, J., Lotfy, R., Wanker, E. E., Rosenmund, C., Liu, F., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2407375121 · Cited by 33 · see citing works
Costello, H., Yamamori, Y., Reeves, S., Schrag, A., Howard, R., & Roiser, J. (2022) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2022-330790 · Cited by 31 · see citing works
MINFLUX fluorescence nanoscopy in biological tissue
Moosmayer, T., Kiszka, K. A., Westphal, V., Pape, J. K., Leutenegger, M., Steffens, H., Grant, S. G. N., Sahl, S. J., & Hell, S. W. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2422020121 · Cited by 26 · see citing works
Self-citationKouvaros, S., Bizup, B. T., Solís, Ó., Kumar, M., Ventriglia, E. N., Curry, F. P., Michaelides, M., & Tzounopoulos, T. (2023) · Science Advances · doi:10.1126/sciadv.adf3525 · Cited by 23 · see citing works
Yang, X., Li, W., Ding, M., Liu, K. J., Qi, Z., & Zhao, Y. (2024) · Metallomics · doi:10.1093/mtomcs/mfae012 · Cited by 21 · see citing works
Synaptic zinc potentiates AMPA receptor function in mouse auditory cortex
Bender, P. T. R., McCollum, M., Boyd-Pratt, H., Mendelson, B. Z., & Anderson, C. T. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112932 · Cited by 18 · see citing works
Liu, Z., Xue, J., Liu, C., Tang, J., Wu, S., Lin, J., Han, J., Zhang, Q., Wu, C., Huang, H., et al. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.373660 · Cited by 19 · see citing works
Krall, R. F., Gale, J. R., Ross, M. M., Tzounopoulos, T., & Aizenman, E. (2022) · Neuroscience Letters · doi:10.1016/j.neulet.2022.136896 · Cited by 16 · see citing works
Widespread co-release of glutamate and GABA throughout the mouse brain
Ceballos, C. C., Ma, L., Qin, M., & Zhong, H. (2024) · Communications Biology · doi:10.1038/s42003-024-07198-y · Cited by 19 · see citing works
Manning, A., Bender, P. T. R., Boyd-Pratt, H., Mendelson, B. Z., Hruska, M., & Anderson, C. T. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0619-24.2024 · Cited by 13 · see citing works
Zhou, Y., Huang, G., Liu, M., Zhang, M., Wu, B., & Gu, J. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1750534 · Cited by 13 · see citing works
Novel Genes Involved in Hypertrophic Cardiomyopathy: Data of Transcriptome and Methylome Profiling
Kiselev, I., Kozin, M., Baulina, N., Pisklova, M., Danilova, L., Zotov, A., Chumakova, O., Zateyshchikov, D., & Favorova, O. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232315280 · Cited by 13 · see citing works
Enhanced synaptic protein visualization by multicolor super-resolution expansion microscopy
Eilts, J., Reinhard, S., Michetschläger, N., Werner, C. D., & Sauer, M. (2023) · Neurophotonics · doi:10.1117/1.nph.10.4.044412 · Cited by 12 · see citing works
On the genesis and unique functions of zinc neuromodulation
Bizup, B. T., & Tzounopoulos, T. (2024) · Journal of Neurophysiology · doi:10.1152/jn.00285.2024 · Cited by 11 · see citing works
Cell-type-specific enhancement of deviance detection by synaptic zinc in the mouse auditory cortex
McCollum, M., Manning, A., Bender, P. T. R., Mendelson, B. Z., & Anderson, C. T. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2405615121 · Cited by 11 · see citing works
Bizup, B. T., Brutsaert, S., Cunningham, C. L., Thathiah, A., & Tzounopoulos, T. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2310561121 · Cited by 10 · see citing works
Cortese, K., Gagliani, M. C., & Raiteri, L. (2023) · Biomedicines · doi:10.3390/biomedicines11123152 · Cited by 8 · see citing works
Yang, Y., Fekete, Á., Arsenault, J., Sengar, A. S., Aı̈toubah, J., Grande, G., Li, A., Salter, E. W., Wang, A., Mark, M. D., et al. (2024) · The Journal of Physiology · doi:10.1113/jp286462 · Cited by 8 · see citing works
Chai, A. (2025) · Frontiers in Neuroscience · doi:10.3389/fnins.2025.1552145 · Cited by 8 · see citing works
Zinc Transporters in Diseases, Including Diabetes and Related Conditions
Xu, W., Wang, X., Gao, Y., Ma, Q., & Li, W. (2025) · Physiology · doi:10.1152/physiol.00026.2025 · Cited by 7 · see citing works
Goral, R. O., Harper, K. M., Bernstein, B. J., Fry, S. A., Lamb, P. W., Moy, S. S., Cushman, J. D., & Yakel, J. L. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1067409 · Cited by 7 · see citing works
Zong, R., Zhang, X., Dong, X., Liu, G., Zhang, J., Gao, Y., Zhang, Z., Ma, Y., Gao, H., & Gamper, N. L. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1375925 · Cited by 7 · see citing works
Marcoli, M., Agnati, L. F., Franco, R., Cortelli, P., Anderlini, D., Guidolin, D., Cervetto, C., & Maura, G. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1038874 · Cited by 7 · see citing works
Metal ion content of internal organs in the calorically restricted Wistar rat
Santos-Díaz, A. I., Solís-López, J., Diaz-Torres, E., Guadarrama-Olmos, J. C., Osorio, B., Kröll, T., Webb, S. M., Hiriart, M., Jiménez‐Estrada, I., & Missirlis, F. (2023) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2023.127182 · Cited by 7 · see citing works
Role of adaptor protein complexes in generating functionally distinct synaptic vesicle pools
Asmerian, H., Alberts, J., Sanetra, A. M., Diaz, A. J., & Silm, K. (2024) · The Journal of Physiology · doi:10.1113/jp286179 · Cited by 5 · see citing works
Manning, A., Mendelson, B. Z., Bender, P. T. R., Bainer, K., Ruby, R., Shifflett, V., Dariano, D. F., Webb, B. A., Geldenhuys, W. J., & Anderson, C. T. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.2067-24.2025 · Cited by 5 · see citing works
ArtiaX: geometric models, camera paths and image processing tools
Roth, P., Ermel, U. H., Moser, D., Arctaedius, G., Wehrheim, M. H., Scheffer, M. P., & Frangakis, A. S. (2025) · Journal of Structural Biology · doi:10.1016/j.jsb.2025.108215 · Cited by 5 · see citing works
Cristofari, P., Desplanque, M., Poirel, O., Hébert, A., Dumas, S., Herzog, É., Danglot, L., Gény, D., Gilles, J.-F., Geeverding, A., et al. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.991732 · Cited by 6 · see citing works
Khaled, H., Ghasemi, Z., Inagaki, M., Patel, K., Naito, Y., Feller, B., Yi, N., Bourojeni, F. B., Lee, A. K., Chofflet, N., et al. (2024) · The EMBO Journal · doi:10.1038/s44318-024-00252-9 · Cited by 4 · see citing works
Wang, W., Chen, J., He, P.-Y., Zhang, M., Cao, H., Palli, S. R., & Sheng, C. (2024) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2024.104243 · Cited by 4 · see citing works
From Blur to Brilliance: The Ascendance of Advanced Microscopy in Neuronal Cell Biology
Campbell, K. R., Hallada, L. P., Huang, Y., & Solecki, D. J. (2024) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-111020-090208 · Cited by 4 · see citing works
Acetylcholine Neurons Become Cholinergic during Three Time Windows in the Developing Mouse Brain
Goral, R. O., Lamb, P. W., & Yakel, J. L. (2024) · eNeuro · doi:10.1523/eneuro.0542-23.2024 · Cited by 5 · see citing works
Xiang, Y., Cui, L., Yao, J., Lou, X., Wu, M., Huo, J., Fan, J., Li, H., Li, K., Wang, X., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-62496-1 · Cited by 3 · see citing works
Lower Zinc but Higher Calcium Content in Rodent Spinal Cord Compared to Brain
Santos-Díaz, A. I., Bizup, B. T., Pantaleón-Gómez, A. K., Osorio, B., Barbier, O. C., Tzounopoulos, T., & Missirlis, F. (2025) · Cells · doi:10.3390/cells14120922 · Cited by 3 · see citing works
Prevalent co-release of glutamate and GABA throughout the mouse brainPreprint
Ceballos, C. C., Ma, L., Qin, M., & Zhong, H. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.27.587069 · Cited by 3 · see citing works
OpenSTED: open-source dynamic intensity minimum system for stimulated emission depletion microscopy
Pierce, S. A., Jacobelli, J., Given, K. S., Macklin, W. B., Gopinath, J. T., Siemens, M. E., Restrepo, D., & Gibson, E. A. (2024) · Neurophotonics · doi:10.1117/1.nph.11.3.034311 · Cited by 2 · see citing works
A new method for isolation and purification of fusion-competent inhibitory synaptic vesicles
Gopal, N., Leitz, J., Wang, C., Esquivies, L. R., Pfuetzner, R. A., & Brünger, A. T. (2024) · Current Research in Physiology · doi:10.1016/j.crphys.2024.100121 · Cited by 2 · see citing works
Strategies and tactics for subcellular targeting of small molecule zinc sensors
McCarthy, W. K., Mrosla, J. M., Pallares, B., & Goldberg, J. M. (2025) · Metallomics · doi:10.1093/mtomcs/mfaf024 · Cited by 1 · see citing works
Synaptic summation shapes information transfer in GABA-glutamate co-transmission
Krubitski, B., Ceballos, C. C., Roachford, T., & Pena, R. F. O. (2025) · Cognitive Neurodynamics · doi:10.1007/s11571-025-10383-2 · Cited by 1 · see citing works
Mesoscopic analysis of GABAergic marker expression in acetylcholine neurons in the whole mouse brain
Goral, R. O., Roy, S., Co, C. A., Wine, R. N., Lamb, P. W., Turner, P. M., McBride, S. J., Usdin, T. B., & Yakel, J. L. (2025) · iScience · doi:10.1016/j.isci.2025.114531 · Cited by 1 · see citing works
An Ultraresponsive Green Biosensor for Robust in Vivo Imaging of Synaptic Zinc Dynamics
Zhang, H., Kumar, M., Correia, R. G., Yang, S., Huang, W., Soares‐Cunha, C., Cody, P. A., Zhang, Y., Tian, X., Zhao, S., et al. (2026) · ACS Sensors · doi:10.1021/acssensors.5c04244 · Cited by 1 · see citing works
Kumar, M., Linnertz, C., Bizup, B. T., Huang, W., Ai, H., & Tzounopoulos, T. (2026) · Science Advances · doi:10.1126/sciadv.aee9298 · Cited by 1 · see citing works
Nasrallah, J. (2024) · Journal of Neuro Psychiatry Reports · doi:10.47363/jnpr/2024(2)102
Pharmacological inhibition of V-ATPase targets mode-switching but not the proton transport cyclePreprint
Kosmidis, E., Fokaeos, M., Shuttle, C. G., Isselstein, M., Cvjetkovic, A., Johnson, P. J., Pedersen, J. L., Jahn, R., Preobraschenski, J., & Stamou, D. G. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.28.679038 · Cited by 1 · see citing works
Self-citationWang, W., Chen, J., Niu, D.-B., Zhang, M., Cao, H., Palli, S. R., & Sheng, C. (2023) · Research Square · doi:10.21203/rs.3.rs-2938066/v1
Elucidation of the zinc binding site in KCNQ channels
Zhang, S., Yang, X., Yang, M., Cao, Y., Shi, S., Gamper, N. L., & Gao, H. (2025) · British Journal of Pharmacology · doi:10.1111/bph.70177
hpGRISZ: a high-performance fluorescent biosensor for in vivo imaging of synaptic zinc dynamicsPreprint
Zhang, H., Kumar, M., Correia, R. G., Yang, S., Huang, W., Soares‐Cunha, C., Cody, P. A., Zhang, Y., Tian, X., Zhao, S., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.06.680726
Electrophysiology in nanoscale compartments
Howell, M. R., Xu, R. J., & Cohen, A. E. (2026) · The Journal of General Physiology · doi:10.1085/jgp.202614011
Does SLC17A9 (VNUT) function as a stand-alone nucleotide and/or phosphate transporter?
Struck, J., Malviya, V., Ganzella, M., Acharya, A., Barg‐Kues, B., Sambandan, S., Ahnert‐Hilger, G., & Jahn, R. (2026) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2026.113360
Self-citationA microfluidics platform for studying ion and solute transport by isolated synaptic vesicles
Upmanyu, N., Olsthoorn, L., Leon, S., Sambandan, S., Perego, E., Mimoso, T., Socrier, L., Cretich, M., Chiari, M., Steinem, C., et al. (2026) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2026.116020
Self-citationWeisbord, J., Cunningham, C. L., Tzounopoulos, T., & Bizup, B. T. (2026) · Cells · doi:10.3390/cells15171554
Milardi, D., Han, J., Lee, H. J., Ding, F., Miller, Y., Faller, P., Bush, A. I., Crouch, P. J., Finkelstein, D. I., Double, K. L., et al. (2026) · Chemical Reviews · doi:10.1021/acs.chemrev.5c00420
Atacak, A., MUTLU, E. G., Acar, G., Baltacı, S. B., Moğulkoç, R., & Baltacı, A. K. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27209329
- Authors
- Upmanyu, N., Jin, J., Emde, H. V. D., Ganzella, M., Bösche, L., Malviya, V. N., Zhuleku, E., Politi, A. Z., Ninov, M., Silbern, I., Leutenegger, M., Urlaub, H., Riedel, D., Preobraschenski, J., Milosevic, I., Hell, S. W., Jahn, R., & Sambandan, S.
- Affiliations
- Max Planck Institute for Multidisciplinary Sciences (DE)
- Max Planck Society (DE)
- Universitätsmedizin Göttingen (DE)
- Max Planck Institute for Medical Research (DE)
- Corresponding author
- Sambandan, Sivakumar
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2022-05
- Volume
- 110
- Issue
- 9
- Pages
- 1483-1497.e7
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W4221118099
- Cited by
- 69
- References
- 77
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 24 · 2023: 16 · 2022: 8
- FWCI
- 6.62
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Neuron (publishedVersion, cc-by)
- PubMed (publishedVersion)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- Funders
- Broad Institute
- Deutsche Forschungsgemeinschaft (EXC 2067, SFB1286, EXC 2067‐1, 390729940, EXC 2067/1390729940)
- Volkswagen Foundation
- Bundesministerium für Bildung und Forschung
- Fraunhofer-Gesellschaft
- Max-Planck-Gesellschaft
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- synaptic vesicles, VGLUT1, ZnT3, vesicle content, neurotransmitter release, single-vesicle imaging
- MeSH terms
- Animals, Mammals, Synapses, Synaptic Vesicles, Neurotransmitter Agents, Membrane Transport Proteins, Neurotransmitter Transport Proteins, Vesicular Glutamate Transport Protein 1
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review