Ultrastructural analysis of wild-type and RIM1α knockout active zones in a large cortical synapse
Open accessPublished version of a preprint
Abstract
Rab3A-interacting molecule (RIM) is crucial for fast Ca 2+ -triggered synaptic vesicle (SV) release in presynaptic active zones (AZs). We investigated hippocampal giant mossy fiber bouton (MFB) AZ architecture in 3D using electron tomography of rapid cryo-immobilized acute brain slices in RIM1α −/− and wild-type mice. In RIM1α −/− , AZs are larger with increased synaptic cleft widths and a 3-fold reduced number of tightly docked SVs (0–2 nm). The distance of tightly docked SVs to the AZ center is increased from 110 to 195 nm, and the width of their electron-dense material between outer SV membrane and AZ membrane is reduced. Furthermore, the SV pool in RIM1α −/− is more heterogeneous. Thus, RIM1α, besides its role in tight SV docking, is crucial for synaptic architecture and vesicle pool organization in MFBs.
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?
The C2A domain of Munc13-1 interacts with the zinc-finger domain of RIM building a heterodimeric complex.
“In contrast, the C2A domain of Munc13-1 interacts with the zinc-finger domain of RIM building a heterodimeric complex [72,89–91].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [91]
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
Scikit-learn: Machine Learning in Python
Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O., Blondel, M., Müller, A., Nothman, J., Louppe, G., et al. (2012) · arXiv · doi:10.48550/arxiv.1201.0490 · Cited by 71,016 · see citing works
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY
Reynolds, E. S. (1963) · The Journal of Cell Biology · doi:10.1083/jcb.17.1.208 · Cited by 24,938 · see citing works
Harris, C. R., Millman, K. J., van der Walt, S. J., Gommers, R., Virtanen, P., Cournapeau, D., Wieser, E., Taylor, J., Berg, S., Smith, N. J., et al. (2020) · Nature · doi:10.1038/s41586-020-2649-2 · Cited by 23,826 · see citing works
Harris, C., Millman, K., van der Walt, S., Gommers, R., Virtanen, P., Cournapeau, D., Wieser, E., Taylor, J., Berg, S., Smith, N., et al. (2020) · RePEc: Research Papers in Economics · Cited by 17,844 · see citing works
Statsmodels: Econometric and Statistical Modeling with Python
Seabold, S., & Perktold, J. (2010) · Proceedings of the Python in Science Conferences · doi:10.25080/majora-92bf1922-011 · Cited by 6,673 · see citing works
NWChem: A comprehensive and scalable open-source solution for large scale molecular simulations
Valiev, M., Bylaska, E. J., Govind, N., Kowalski, K., Straatsma, T. P., van Dam, H. J. J., Wang, D., Nieplocha, J., Aprà, E., Windus, T. L., et al. (2010) · Computer Physics Communications · doi:10.1016/j.cpc.2010.04.018 · Cited by 5,794 · see citing works
Computer visualization of three-dimensional image data using IMOD.
Kremer, J. R., Mastronarde, D., & Mcintosh, J. (1996) · Journal of Structural Biology · doi:10.1006/jsbi.1996.0013 · Cited by 5,770 · see citing works
Automated electron microscope tomography using robust prediction of specimen movements.
Mastronarde, D. (2005) · Journal of Structural Biology · doi:10.1016/j.jsb.2005.07.007 · Cited by 5,446 · see citing works
Jupyter Notebooks – a publishing format for reproducible computational workflows
Kluyver, T. A., Ragan-Kelley, B., Fernando, P., Granger, B., Bussonnier, M., Frederic, J., Kelley, K., Hamrick, J. B., Grout, J., Corlay, S., et al. (2016) · IOS Press eBooks · doi:10.3233/978-1-61499-649-1-87 · Cited by 3,191 · see citing works
Jonas, P., Major, G., & Sakmann, B. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019965 · Cited by 720 · see citing works
Differential Control of Learning and Anxiety along the Dorsoventral Axis of the Dentate Gyrus
Kheirbek, M. A., Drew, L. J., Burghardt, N. S., Costantini, D. O., Tannenholz, L., Ahmari, S. E., Zeng, H., Fenton, A. A., & Hen, R. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.038 · Cited by 713 · see citing works
Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion
Wang, Y., Okamoto, M., Schmitz, F., Hofmann, K., & Südhof, T. C. (1997) · Nature · doi:10.1038/41580 · Cited by 684 · see citing works
A trans-synaptic nanocolumn aligns neurotransmitter release to receptors
Tang, A.-H., Chen, H., Li, T. P., Metzbower, S. R., MacGillavry, H. D., & Blanpied, T. A. (2016) · Nature · doi:10.1038/nature19058 · Cited by 677 · see citing works
Synaptic plasticity at hippocampal mossy fibre synapses
Nicoll, R. A., & Schmitz, D. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1786 · Cited by 653 · see citing works
Mitochondria at the neuronal presynapse in health and disease
Devine, M. J., & Kittler, J. T. (2018) · Nature reviews. Neuroscience · doi:10.1038/nrn.2017.170 · Cited by 615 · see citing works
RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction
Kaeser, P. S., Deng, L., Wang, Y., Dulubova, I., Liu, X., Rizo, J., & Südhof, T. C. (2011) · Cell · doi:10.1016/j.cell.2010.12.029 · Cited by 607 · see citing works
Ultrafast endocytosis at mouse hippocampal synapses
Watanabe, S., Rost, B. R., Camacho-Pérez, M., Davis, M. W., Söhl-Kielczynski, B., Rosenmund, C., & Jorgensen, E. M. (2013) · Nature · doi:10.1038/nature12809 · Cited by 607 · see citing works
Amaral, D. G., & Dent, J. A. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901950106 · Cited by 606 · see citing works
RIM1α forms a protein scaffold for regulating neurotransmitter release at the active zone
Schoch, S., Castillo, P. E., Jo, T., Mukherjee, K., Geppert, M., Wang, Y., Schmitz, F., Malenka, R. C., & Südhof, T. C. (2002) · Nature · doi:10.1038/415321a · Cited by 579 · see citing works
Self-citationA liquid phase of synapsin and lipid vesicles
Milovanović, D., Wu, Y., Bian, X., & Camilli, P. V. D. (2018) · Science · doi:10.1126/science.aat5671 · Cited by 494 · see citing works
Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo
Henze, D. A., Wittner, L., & Buzsáki, G. (2002) · Nature Neuroscience · doi:10.1038/nn887 · Cited by 480 · see citing works
Electron Microscopy of Synaptic Contacts on Dendrite Spines of the Cerebral Cortex
Gray, E. G. (1959) · Nature · doi:10.1038/1831592a0 · Cited by 443 · see citing works
Ultrastructural analysis of adult mouse neocortex comparing aldehyde perfusion with cryo fixation
Korogod, N., Petersen, C. C., & Knott, G. W. (2015) · eLife · doi:10.7554/elife.05793 · Cited by 408 · see citing works
The Morphological and Molecular Nature of Synaptic Vesicle Priming at Presynaptic Active Zones
Imig, C., Min, S.-W., Krinner, S., Arancillo, M., Rosenmund, C., Südhof, T. C., Rhee, J., Brose, N., & Cooper, B. H. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.009 · Cited by 389 · see citing works
RIM1α is required for presynaptic long-term potentiation
Castillo, P. E., Schoch, S., Schmitz, F., Südhof, T. C., & Malenka, R. C. (2002) · Nature · doi:10.1038/415327a · Cited by 389 · see citing works
Self-citationThe architecture of active zone material at the frog's neuromuscular junction
Harlow, M. L., Ress, D., Stoschek, A., Marshall, R. M., & McMahan, U. J. (2001) · Nature · doi:10.1038/35054000 · Cited by 388 · see citing works
RIM determines Ca2+ channel density and vesicle docking at the presynaptic active zone
Han, Y., Kaeser, P. S., Südhof, T. C., & Schneggenburger, R. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.014 · Cited by 354 · see citing works
The Structural Organization of the Readily Releasable Pool of Synaptic Vesicles
Rizzoli, S. O., & Betz, W. J. (2004) · Science · doi:10.1126/science.1094682 · Cited by 340 · see citing works
Three-Dimensional Architecture of Presynaptic Terminal Cytomatrix
Siksou, L., Rostaing, P., Lechaire, J., Boudier, T., Ohtsuka, T., Fejtová, A., Kao, H., Greengard, P., Gundelfinger, E. D., Triller, A., et al. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1773-07.2007 · Cited by 329 · see citing works
Patch-clamp recording from mossy fiber terminals in hippocampal slices
Bischofberger, J., Engel, D., Li, L., Geiger, J. R., & Jónás, P. (2006) · Nature Protocols · doi:10.1038/nprot.2006.312 · Cited by 315 · see citing works
RIM Binding Proteins (RBPs) Couple Rab3-Interacting Molecules (RIMs) to Voltage-Gated Ca2+ Channels
Hibino, H., Pironkova, R., Onwumere, O., Vologodskaia, M., Hudspeth, A. J., & Lesage, F. (2002) · Neuron · doi:10.1016/s0896-6273(02)00667-0 · Cited by 309 · see citing works
RIM Proteins Activate Vesicle Priming by Reversing Autoinhibitory Homodimerization of Munc13
Deng, L., Kaeser, P. S., Xu, W., & Südhof, T. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.005 · Cited by 287 · see citing works
RIM1 confers sustained activity and neurotransmitter vesicle anchoring to presynaptic Ca2+ channels
Kiyonaka, S., Wakamori, M., Miki, T., Uriu, Y., Nonaka, M., Bito, H., Beedle, A., Mori, E., Hara, Y., Waard, M. D., et al. (2007) · Nature Neuroscience · doi:10.1038/nn1904 · Cited by 262 · see citing works
Wang, Y., Liu, X., Biederer, T., & Südhof, T. C. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182532999 · Cited by 256 · see citing works
Structural determinants of transmission at large hippocampal mossy fiber synapses
Rollenhagen, A., Sätzler, K., Rodríguez, E. P., Jonas, P., Frotscher, M., & Lübke, J. H. R. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1946-07.2007 · Cited by 246 · see citing works
The readily releasable pool of synaptic vesicles
Kaeser, P. S., & Regehr, W. G. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.12.012 · Cited by 231 · see citing works
RIM and RIM-BP Form Presynaptic Active-Zone-like Condensates via Phase Separation.
Wu, X., Cai, Q., Shen, Z., Chen, X., Zeng, M.-L., Du, S.-W., & Zhang, M.-J. (2019) · Molecules and Cells · doi:10.1016/j.molcel.2018.12.007 · Cited by 216 · see citing works
Dynamically Primed Synaptic Vesicle States: Key to Understand Synaptic Short-Term Plasticity
Neher, E., & Brose, N. (2018) · Neuron · doi:10.1016/j.neuron.2018.11.024 · Cited by 210 · see citing works
Vyleta, N. P., & Jonas, P. (2014) · Science · doi:10.1126/science.1244811 · Cited by 189 · see citing works
A large pool of releasable vesicles in a cortical glutamatergic synapse
Hallermann, S., Pawlu, C., Jonas, P., & Heckmann, M. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1432836100 · Cited by 181 · see citing works
Self-citationRIM Controls Homeostatic Plasticity through Modulation of the Readily-Releasable Vesicle Pool
Müller, M., Liu, K. S. Y., Sigrist, S. J., & Davis, G. W. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0981-12.2012 · Cited by 179 · see citing works
Wilke, S. A., Antonios, J. K., Bushong, E. A., Badkoobehi, A., Malek, E., Hwang, M., Terada, M., Ellisman, M. H., & Ghosh, A. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1600-12.2013 · Cited by 179 · see citing works
The optimal height of the synaptic cleft
Savtchenko, L. P., & Rusakov, D. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606636104 · Cited by 177 · see citing works
Galimberti, I., Gogolla, N., Alberi, S., Santos, A. F., Müller, D., & Caroni, P. (2006) · Neuron · doi:10.1016/j.neuron.2006.04.026 · Cited by 163 · see citing works
Analysis of synaptic ultrastructure without fixative using high‐pressure freezing and tomography
Rostaing, P., Réal, É., Siksou, L., Lechaire, J. P., Boudier, T., Boeckers, T. M., Gertler, F. B., Gundelfinger, E. D., Triller, A., & Marty, S. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05234.x · Cited by 152 · see citing works
Fusion Competent Synaptic Vesicles Persist upon Active Zone Disruption and Loss of Vesicle Docking
Wang, S. S. H., Held, R. G., Wong, M. Y., Liu, C., Karakhanyan, A., & Kaeser, P. S. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.005 · Cited by 143 · see citing works
The Presynaptic Active Zone Protein RIM1α Is Critical for Normal Learning and Memory
Powell, C. M., Schoch, S., Monteggia, L., Barrot, M., Matos, M. F., Feldmann, N., Südhof, T. C., & Nestler, E. J. (2004) · Neuron · doi:10.1016/s0896-6273(04)00146-1 · Cited by 143 · see citing works
Self-citationSynaptic vesicles transiently dock to refill release sites
Kusick, G. F., Chin, M., Raychaudhuri, S., Lippmann, K., Adula, K. P., Hujber, E. J., Vu, T., Davis, M. W., Jorgensen, E. M., & Watanabe, S. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00716-1 · Cited by 138 · see citing works
Cryo–electron tomography reveals a critical role of RIM1α in synaptic vesicle tethering
Fernández‐Busnadiego, R., Asano, S. M., Oprişoreanu, A., Sakata, E., Doengi, M., Kochovski, Z., Zürner, M., Stein, V., Schoch, S., Baumeister, W. P., et al. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201206063 · Cited by 128 · see citing works
Self-citationRedundant functions of RIM1α and RIM2α in Ca2+‐triggered neurotransmitter release
Schoch, S., Mittelstaedt, T., Kaeser, P. S., Padgett, D., Feldmann, N., Chevaleyre, V., Castillo, P. E., Hammer, R. E., Han, W., Schmitz, F., et al. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601425 · Cited by 126 · see citing works
Self-citationQuantal transmission at mossy fibre targets in the CA3 region of the rat hippocampus
Lawrence, J. J., Grinspan, Z. M., & McBain, C. J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.049551 · Cited by 125 · see citing works
Synaptic vesicle pools are a major hidden resting metabolic burden of nerve terminals
Pulido, C., & Ryan, T. A. (2021) · Science Advances · doi:10.1126/sciadv.abi9027 · Cited by 120 · see citing works
Variations in electrophysiological properties of hippocampal neurons in different subfields
Masukawa, L. M., Benardo, L. S., & Prince, D. A. (1982) · Brain Research · doi:10.1016/0006-8993(82)90320-1 · Cited by 117 · see citing works
Stigloher, C., Zhan, H., Zhen, M., Richmond, J. E., & Bessereau, J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6164-10.2011 · Cited by 115 · see citing works
Self-citationRIM genes differentially contribute to organizing presynaptic release sites
Kaeser, P. S., Deng, L., Fan, M., & Südhof, T. C. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209318109 · Cited by 115 · see citing works
Vandael, D., Borges-Merjane, C., Zhang, X., & Jonas, P. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.013 · Cited by 114 · see citing works
Assembly of the presynaptic active zone
Emperador-Melero, J., & Kaeser, P. S. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.03.008 · Cited by 109 · see citing works
Andrews-Zwilling, Y. S., Kawabe, H., Reim, K., Varoqueaux, F., & Brose, N. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m601421200 · Cited by 103 · see citing works
RIM Promotes Calcium Channel Accumulation at Active Zones of the Drosophila Neuromuscular Junction
Graf, E., Valakh, V., Wright, C. M., Wu, C.-L., Liu, Z., Zhang, Y. Q., & Diantonio, A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0965-12.2012 · Cited by 96 · see citing works
Heterodimerization of Munc13 C2A domain with RIM regulates synaptic vesicle docking and priming
Camacho, M., Basu, J., Trimbuch, T., Chang, S., Pulido-Lozano, C., Chang, S.-S., Duluvova, I., Abo-Rady, M., Rizo, J., & Rosenmund, C. (2017) · Nature Communications · doi:10.1038/ncomms15293 · Cited by 95 · see citing works
Plasticity-dependent, full detonation at hippocampal mossy fiber-CA3 pyramidal neuron synapses
Vyleta, N. P., Borges-Merjane, C., & Jonas, P. (2016) · eLife · doi:10.7554/elife.17977 · Cited by 91 · see citing works
Hypothesis – buttressed rings assemble, clamp, and release SNAREpins for synaptic transmission
Rothman, J. E., Krishnakumar, S. S., Grushin, K. S., & Pincet, F. (2017) · FEBS Letters · doi:10.1002/1873-3468.12874 · Cited by 85 · see citing works
α-Neurexins Together with α2δ-1 Auxiliary Subunits Regulate Ca 2+ Influx through Ca v 2.1 Channels
Brockhaus, J., Schreitmüller, M., Repetto, D., Klatt, O., Reißner, C., Elmslie, K. S., Heine, M., & Missler, M. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0511-18.2018 · Cited by 82 · see citing works
Held, R. G., Liu, C., & Kaeser, P. S. (2016) · eLife · doi:10.7554/elife.14862 · Cited by 67 · see citing works
Ultrastructural Correlates of Presynaptic Functional Heterogeneity in Hippocampal Synapses
Maus, L., Lee, C., Altas, B., Sertel, S. M., Weyand, K., Rizzoli, S. O., Rhee, J., Brose, N., Imig, C., & Cooper, B. H. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.083 · Cited by 67 · see citing works
Grushin, K., Kalyana Sundaram, R. V., Sindelar, C. V., & Rothman, J. E. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2121259119 · Cited by 66 · see citing works
Imig, C., López-Murcia, F. J., Maus, L., García-Plaza, I. H., Mortensen, L. S., Schwark, M., Schwarze, V., Angibaud, J., Nägerl, U. V., Taschenberger, H., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.09.004 · Cited by 66 · see citing works
The mossy fiber bouton: the "common" or the "unique" synapse?
Rollenhagen, A. (2010) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2010.00002 · Cited by 66 · see citing works
Synapsins and the Synaptic Vesicle Reserve Pool: Floats or Anchors?
Zhang, M., & Augustine, G. J. (2021) · Cells · doi:10.3390/cells10030658 · Cited by 65 · see citing works
Trans-synaptic assemblies link synaptic vesicles and neuroreceptors
Martínez-Sánchez, A., Laugks, U., Kochovski, Z., Papantoniou, C., Zinzula, L., Baumeister, W. P., & Lučić, V. (2021) · Science Advances · doi:10.1126/sciadv.abe6204 · Cited by 62 · see citing works
Borges-Merjane, C., Kim, O., & Jonas, P. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.022 · Cited by 60 · see citing works
RIM C2B Domains Target Presynaptic Active Zone Functions to PIP2-Containing Membranes
de Jong, A. P. H., Roggero, C. M., Ho, M., Wong, M. Y., Brautigam, C. A., Rizo, J., & Kaeser, P. S. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.011 · Cited by 59 · see citing works
Structural plasticity of hippocampal mossy fiber synapses as revealed by high‐pressure freezing
Zhao, S., Studer, D., Chai, X., Graber, W. A., Brose, N., Nestel, S., Young, C. C., Rodriguez, E., Saetzler, K., & Frotscher, M. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23040 · Cited by 56 · see citing works
Active zone compaction correlates with presynaptic homeostatic potentiation
Mrestani, A., Pauli, M., Kollmannsberger, P., Repp, F., Kittel, R. J., Eilers, J., Doose, S., Sauer, M., Sirén, A., Heckmann, M., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109770 · Cited by 54 · see citing works
Self-citationBrockmann, M. M., Zarebidaki, F., Camacho, M., Grauel, M. K., Trimbuch, T., Südhof, T. C., & Rosenmund, C. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107960 · Cited by 53 · see citing works
Art and Science of the Cellular Mesoscale
Goodsell, D. S., Olson, A. J., & Forli, S. (2020) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.02.010 · Cited by 46 · see citing works
Disentangling the roles of RIM and Munc13 in synaptic vesicle localization and neurotransmission
Zarebidaki, F., Camacho, M., Brockmann, M. M., Trimbuch, T., Herman, M. A., & Rosenmund, C. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.1922-20.2020 · Cited by 37 · see citing works
Miki, T., Kiyonaka, S., Uriu, Y., Waard, M. D., Wakamori, M., Beedle, A., Campbell, K., & Mori, Y. (2007) · Channels · doi:10.4161/chan.4660 · Cited by 34 · see citing works
Orlando, M., Dvorzhak, A., Bruentgens, F., Maglione, M., Rost, B. R., Sigrist, S. J., Breustedt, J., & Schmitz, D. (2021) · PLOS Biology · doi:10.1371/journal.pbio.3001149 · Cited by 30 · see citing works
Role of RIM1α in short- and long-term synaptic plasticity at cerebellar parallel fibres
Kintscher, M., Wozny, C., Johenning, F., Schmitz, D., & Breustedt, J. (2013) · Nature Communications · doi:10.1038/ncomms3392 · Cited by 29 · see citing works
Synapsin- and Actin-Dependent Frequency Enhancement in Mouse Hippocampal Mossy Fiber Synapses
Owe, S. G., Jensen, V., Evergren, E., Ruiz, A. J., Shupliakov, O., Kullmann, D. M., Storm‐Mathisen, J., Walaas, S. I., Hvalby, Ø., & Bergersen, L. H. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn101 · Cited by 24 · see citing works
Butola, T., Alvanos, T., Hintze, A., Koppensteiner, P., Kleindienst, D., Shigemoto, R., Wichmann, C., & Moser, T. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0586-21.2021 · Cited by 22 · see citing works
Pauli, M., Paul, M. M., Proppert, S., Mrestani, A., Sharifi, M., Repp, F., Kürzinger, L., Kollmannsberger, P., Sauer, M., Heckmann, M., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-01939-z · Cited by 12 · see citing works
Self-citationThe human cognition-enhancing CORD7 mutation increases active zone number and synaptic release
Paul, M. M., Dannhäuser, S., Morris, L., Mrestani, A., Hübsch, M., Gehring, J., Hatzopoulos, G. N., Pauli, M., Auger, G. M., Bornschein, G., et al. (2022) · Brain · doi:10.1093/brain/awac011 · Cited by 11 · see citing works
Self-citationAnalysis of Specificity in Immunoelectron Microscopy
Hacker, C., & Lucocq, J. M. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-776-1_14 · Cited by 11 · see citing works
Markert, S. M., Skoruppa, M., Yu, B., Mulcahy, B., Zhen, M., 高尚邦, Sendtner, M., & Stigloher, C. (2020) · Zenodo (CERN European Organization for Nuclear Research) · doi:10.5061/dryad.9ghx3ffg0 · Cited by 7 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- van Rossum, G., and de Boer, J. (1991). Linking a Stub Generator (AIL) to a Prototyping Language (Python). Paper presented at: EurOpen Conference Proceedings (May 20-24, 1991) (Tromso, Norway).
Cited by
Sorted by citations
Structure, biophysics, and circuit function of a “giant” cortical presynaptic terminal
Vandael, D., & Jonas, P. (2024) · Science · doi:10.1126/science.adg6757 · Cited by 45 · see citing works
“Kiss-shrink-run” unifies mechanisms for synaptic vesicle exocytosis and hyperfast recycling
Tao, C.-L., Tian, C.-L., Liu, Y.-T., Lu, Z.-H., Qi, L., Li, X., Li, C., Shen, X., Gu, M., Huang, W.-L., et al. (2025) · Science · doi:10.1126/science.ads7954 · Cited by 29 · see citing works
Ehrenreich, H., Gassmann, M., Poustka, L., Burtscher, M., Hammermann, P., Sirén, A., Nave, K., & Miskowiak, K. W. (2023) · Neuroprotection/Neuroprotection (Chichester, England. Print) · doi:10.1002/nep3.15 · Cited by 19 · see citing works
Self-citationKim, O., Okamoto, Y., Kaufmann, W. A., Brose, N., Shigemoto, R., & Jonas, P. (2024) · PLOS Biology · doi:10.1371/journal.pbio.3002879 · Cited by 15 · see citing works
“In contrast, the C 2 A domain of Munc13-1 interacts with the zinc-finger domain of RIM building a heterodimeric complex [72,89–91].”
Short term plasticity at hippocampal mossy fiber synapses
Marneffe, C., Moreira-de-Sá, A., Lecomte, S., Erhardt, A., & Mulle, C. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.09.044 · Cited by 13 · see citing works
Suzuki, C., Yamaguchi, J., Mitsui, S., Sanada, T., Trejo, J. A. O., Kakuta, S., Tanaka, K., Suda, Y., Hatano, T., Hattori, N., et al. (2024) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2024.167494 · Cited by 4 · see citing works
Lippmann, K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25136862 · Cited by 4 · see citing works
Visualizing Presynaptic Active Zones and Synaptic Vesicles
Heckmann, M., & Pauli, M. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.901341 · Cited by 3 · see citing works
Self-citationMrestani, A., Lichter, K., Sirén, A., Heckmann, M., Paul, M. M., & Pauli, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032128 · Cited by 1 · see citing works
Self-citationThe flexible synapse – How mossy fiber architecture adapts to changing needs
Bruentgens, F., Schmitz, D., & Orlando, M. (2026) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2026.102882 · Cited by 1 · see citing works
Lichter, K. (2025) · Science · doi:10.1126/science.aec0091
Self-citationLin, L.-H., Li, W., Wu, Q.-Y., Li, S., Ma, X.-X., Xu, Y., Deng, S.-F., Zhang, B., & Liu, J. H. (2025) · Neuroscience Bulletin · doi:10.1007/s12264-025-01528-8
Morphofunctional Features of Hippocampal Mossy Fibers
Safiulina, V. F. (2025) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093025060213
Ion‐ and Temperature‐Programmable Reconfiguration of Subcompartments in Synthetic Cells
Xu, Z., & Schwille, P. (2026) · ChemBioChem · doi:10.1002/cbic.202500928
- Authors
- Lichter, K., Paul, M. M., Pauli, M., Schoch, S., Kollmannsberger, P., Stigloher, C., Heckmann, M., & Sirén, A.-L.
- Affiliations
- University of Würzburg (DE)
- University Hospital Bonn (DE)
- Corresponding author
- Stigloher, Christian
- Heckmann, Manfred
- Sirén, Anna-Leena
- ORCID
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2022-09
- Volume
- 40
- Issue
- 12
- Pages
- 111382
- ISSN
- 2211-1247 (ISSN-L)
- OpenAlex
- W4296478994
- Cited by
- 15
- References
- 87
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 6 · 2023: 2 · 2022: 1
- FWCI
- 1.43
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- Online Publication Service of Würzburg University (Würzburg University) (submittedVersion, cc-by-nc-nd)
- Funders
- Julius Maximilians University Würzburg
- Deutsche Forschungsgemeinschaft (218894163, CRC 166)
- Interdisziplinäres Zentrum für Klinische Forschung, Universitätsklinikum Würzburg
- European Molecular Biology Laboratory
- 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
- active zone, synaptic vesicle docking, hippocampus, synaptic vesicle pools, synaptic cleft width, knockout mice
- MeSH terms
- Animals, Synaptic Transmission, Synapses, Synaptic Vesicles, Presynaptic Terminals, Mossy Fibers, Hippocampal, Mice
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