Distinct active zone protein machineries mediate Ca2+ channel clustering and vesicle priming at hippocampal synapses
Open accessAbstract
Action potentials trigger neurotransmitter release at the presynaptic active zone with spatiotemporal precision. This is supported by protein machinery that mediates synaptic vesicle priming and clustering of Ca V 2 Ca 2+ channels nearby. One model posits that scaffolding proteins directly tether vesicles to Ca V 2s; however, here we find that at mouse hippocampal synapses, Ca V 2 clustering and vesicle priming are executed by separate machineries. Ca V 2 nanoclusters are positioned at variable distances from those of the priming protein Munc13. The active zone organizer RIM anchors both proteins but distinct interaction motifs independently execute these functions. In transfected cells, Liprin-α and RIM form co-assemblies that are separate from Ca V 2-organizing complexes. At synapses, Liprin-α1-Liprin-α4 knockout impairs vesicle priming but not Ca V 2 clustering. The cell adhesion protein PTPσ recruits Liprin-α, RIM and Munc13 into priming complexes without co-clustering Ca V 2s. We conclude that active zones consist of distinct machineries to organize Ca V 2s and prime vesicles, and Liprin-α and PTPσ specifically support priming site assembly.
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?
RIM1/2 recruits Munc13-1s to active zones and interacts with other active zone components to enable exocytosis.
“RIM1/2 recruits Munc13-1s to AZs [72,73] and interacts with other AZ components to enable exocytosis [73–76].”
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 [76]
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
1 retracted
Chen, L. Y., Jiang, M., Zhang, B., Gökçe, Ö., & Südhof, T. C. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.011 · Cited by 207 · see citing works
RetractedMultiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT
Jungmann, R., Avendaño, M. S., Woehrstein, J. B., Dai, M., Shih, W. M., & Yin, P. (2014) · Nature Methods · doi:10.1038/nmeth.2835 · Cited by 1,137 · see citing works
Südhof, T. C. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.012 · Cited by 1,062 · 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
Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles
Augustin, I., Rosenmund, C., Südhof, T. C., & Brose, N. (1999) · Nature · doi:10.1038/22768 · Cited by 787 · see citing works
Bruchpilot Promotes Active Zone Assembly, Ca <sup>2+</sup> Channel Clustering, and Vesicle Release
Kittel, R. J., Wichmann, C., Rasse, T. M., Fouquet, W., Schmidt, M., Schmid, A., Wagh, D. A., Pawlu, C., Kellner, R. R., Willig, K. I., et al. (2006) · Science · doi:10.1126/science.1126308 · Cited by 772 · see citing works
Different types of calcium channels mediate central synaptic transmission
Takahashi, T., & Momiyama, A. (1993) · Nature · doi:10.1038/366156a0 · Cited by 755 · 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 · cited 6× · see citing works
“Autocorrelation was calculated as previously described 55,82 , modified for 2d localizations.”
InfluentialSelf-citationRIM 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
Self-citationRIM1α 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
Rational design of true monomeric and bright photoactivatable fluorescent proteins
Zhang, M., Chang, H., Zhang, Y., Yu, J., Wu, L., Ji, W., Chen, J., Liu, B., Lu, J., Liu, Y., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2021 · Cited by 511 · see citing works
Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming
Betz, A., Thakur, P., Junge, H. J., Ashery, U., Rhee, J.-S., Scheuss, V., Rosenmund, C., Rettig, J., & Brose, N. (2001) · Neuron · doi:10.1016/s0896-6273(01)00272-0 · Cited by 425 · see citing works
Reconstitution of the Vital Functions of Munc18 and Munc13 in Neurotransmitter Release
Ma, C., Su, L., Seven, A. B., Xu, Y., & Rizo, J. (2012) · Science · doi:10.1126/science.1230473 · Cited by 409 · see citing works
Rozov, A., Burnashev, N., Sakmann, B., & Neher, E. (2001) · Journal of Physiology · doi:10.1111/j.1469-7793.2001.0807h.x · Cited by 392 · see citing works
The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans
Zhen, M., & Jin, Y. (1999) · Nature · doi:10.1038/43886 · Cited by 374 · see citing works
Dymecki, S. M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.12.6191 · Cited by 361 · 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
Self-citationRIM 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-Binding Protein, a Central Part of the Active Zone, Is Essential for Neurotransmitter Release
Liu, K. S. Y., Siebert, M., Mertel, S., Knoche, E., Wegener, S., Wichmann, C., Matkovic, T., Muhammad, K., Depner, H., Mettke, C., et al. (2011) · Science · doi:10.1126/science.1212991 · Cited by 306 · see citing works
Drosophila Liprin-α and the Receptor Phosphatase Dlar Control Synapse Morphogenesis
Kaufmann, N., DeProto, J., Ranjan, R., Wan, H., & Vactor, D. V. (2002) · Neuron · doi:10.1016/s0896-6273(02)00643-8 · Cited by 302 · see citing works
Piccolo, a presynaptic zinc finger protein structurally related to bassoon
Fenster, S. D., Chung, W. J., Zhai, R., Cases-Langhoff, C., Voss, B., Garner, A. M., Kaempf, U., Kindler, S., Gundelfinger, E. D., & Garner, C. C. (2000) · Neuron · doi:10.1016/s0896-6273(00)80883-1 · Cited by 295 · see citing works
Liprins, a Family of LAR Transmembrane Protein-tyrosine Phosphatase-interacting Proteins
Serra‐Pages, C., Medley, Q. G., Tang, M., Hart, A. C., & Streuli, M. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.25.15611 · Cited by 292 · see citing works
A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity?
Dulubova, I., Lou, X., Lu, J., Huryeva, I., Alam, A., Schneggenburger, R., Südhof, T. C., & Rizo, J. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600753 · Cited by 289 · 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
Self-citationRIM1 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
Protein tyrosine phosphatases PTPδ, PTPσ, and LAR: presynaptic hubs for synapse organization
Takahashi, H., & Craig, A. M. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.06.002 · Cited by 257 · see citing works
Dopamine Secretion Is Mediated by Sparse Active Zone-like Release Sites
Liu, C., Kershberg, L., Wang, J., Schneeberger, S., & Kaeser, P. S. (2018) · Cell · doi:10.1016/j.cell.2018.01.008 · Cited by 249 · see citing works
Self-citationNakamura, Y., Harada, H., Kamasawa, N., Matsui, K., Rothman, J. S., Shigemoto, R., Silver, R. A., DiGregorio, D. A., & Takahashi, T. (2015) · Neuron · doi:10.1016/j.neuron.2014.11.019 · Cited by 245 · see citing works
Synaptic weight set by Munc13-1 supramolecular assemblies
Sakamoto, H., Ariyoshi, T., Kimpara, N., Sugao, K., Taiko, I., Takikawa, K., Asanuma, D., Namiki, S., & Hirose, K. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0041-9 · Cited by 235 · 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
Self-citationActive zone scaffolds differentially accumulate Unc13 isoforms to tune Ca2+ channel–vesicle coupling
Böhme, M. A., Beis, C., Reddy‐Alla, S., Reynolds, E., Mampell, M. M., Grasskamp, A. T., Lützkendorf, J., Bergeron, D. D., Driller, J. H., Babikir, H. A., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4364 · Cited by 221 · see citing works
SYD-2 Liprin-α organizes presynaptic active zone formation through ELKS
Dai, Y., Taru, H., Deken, S. L., Grill, B., Ackley, B., Nonet, M. L., & Jin, Y. (2006) · Nature Neuroscience · doi:10.1038/nn1808 · Cited by 218 · 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
Up to 100-fold speed-up and multiplexing in optimized DNA-PAINT
Strauss, S., & Jungmann, R. (2020) · Nature Methods · doi:10.1038/s41592-020-0869-x · Cited by 198 · see citing works
Mukherjee, K., Yang, X., Gerber, S. H., Kwon, H.-B., Ho, A., Castillo, P. E., Liu, X., & Südhof, T. C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002307107 · Cited by 195 · see citing works
Vyleta, N. P., & Jonas, P. (2014) · Science · doi:10.1126/science.1244811 · Cited by 189 · see citing works
Cao, Y. Q., Piedras-Renterı́a, E. S., Smith, G. B., Chen, G., Harata, N. C., & Tsien, R. W. (2004) · Neuron · doi:10.1016/j.neuron.2004.07.014 · Cited by 185 · see citing works
Ko, J., Na, M., Kim, S.-H., Lee, J.-R., & Kim, E. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m307561200 · Cited by 185 · see citing works
Bassoon Specifically Controls Presynaptic P/Q-type Ca2+ Channels via RIM-Binding Protein
Davydova, D., Marini, C., King, C., Klueva, J., Bischof, F., Romorini, S., Montenegro‐Venegas, C., Heine, M., Schneider, R., Schröder, M. S., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.012 · Cited by 172 · see citing works
Assembly of synaptic active zones requires phase separation of scaffold molecules
McDonald, N. A., Fetter, R. D., & Shen, K. (2020) · Nature · doi:10.1038/s41586-020-2942-0 · Cited by 162 · see citing works
How to Make an Active Zone: Unexpected Universal Functional Redundancy between RIMs and RIM-BPs
Acuna, C., Liu, X., & Südhof, T. C. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.042 · Cited by 154 · see citing works
Sheng, Z.-H., Westenbroek, R., & Catterall, W. (1998) · Journal of Bioenergetics and Biomembranes · doi:10.1023/a:1021985521748 · Cited by 145 · 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
Self-citationReddy‐Alla, S., Böhme, M. A., Reynolds, E., Beis, C., Grasskamp, A. T., Mampell, M. M., Maglione, M., Jusyte, M., Rey, U., Babikir, H. A., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.08.016 · Cited by 141 · see citing works
Rebola, N., Reva, M., Kirizs, T., Szoboszlay, M., Lőrincz, A., Moneron, G., Nusser, Z., & DiGregorio, D. A. (2019) · Neuron · doi:10.1016/j.neuron.2019.08.014 · Cited by 136 · see citing works
Vesicle Tethering on the Surface of Phase-Separated Active Zone Condensates
Wu, X., Ganzella, M., Zhou, J., Zhu, S., Jahn, R., & Zhang, M. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.10.029 · Cited by 119 · see citing works
Ackley, B. D., Harrington, R. J., Hudson, M. L., Williams, L., Kenyon, C. J., Chisholm, A. D., & Jin, Y. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2010-05.2005 · Cited by 113 · 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
Self-citationRIM-BPs Mediate Tight Coupling of Action Potentials to Ca 2+ -Triggered Neurotransmitter Release
Acuna, C., Liu, X., Gonzalez-Suarez, A. D., & Südhof, T. C. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.027 · Cited by 104 · see citing works
Emperador-Melero, J., Wong, M. Y., Wang, S. S. H., de Nola, G., Nyitrai, H., Kirchhausen, T. L., & Kaeser, P. S. (2021) · Nature Communications · doi:10.1038/s41467-021-23116-w · Cited by 104 · see citing works
Self-citationELKS2α/CAST deletion selectively increases neurotransmitter release at inhibitory synapses
Kaeser, P. S., Deng, L., Chávez, A. E., Liu, X., Castillo, P. E., & Südhof, T. C. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.019 · Cited by 102 · see citing works
Self-citationKaeser, P. S., Kwon, H.-B., Chiu, C.-Y. Q., Deng, L., Castillo, P., & Südhof, T. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3235-08.2008 · Cited by 97 · see citing works
Self-citationSubsynaptic positioning of AMPARs by LRRTM2 controls synaptic strength
Ramsey, A. M., Tang, A., LeGates, T. A., Gou, X., Carbone, B. E., Thompson, S. M., Biederer, T., & Blanpied, T. A. (2021) · Science Advances · doi:10.1126/sciadv.abf3126 · Cited by 90 · see citing works
Self-citationGrauel, M., Maglione, M., Reddy-Alla, S., Willmes, C., Brockmann, M. M., Trimbuch, T., Rosenmund, T., Pangalos, M., Vardar, G., Stumpf, A., et al. (2016) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1605256113 · Cited by 89 · see citing works
Synapse and active zone assembly in the absence of presynaptic Ca2+ channels and Ca2+ entry
Held, R. G., Liu, C.-L., Ma, K.-P., Ramsey, A. M., Tarr, T. B., de Nola, G., Wang, S.-S. H., Wang, J., van den Maagdenberg, A. M., Schneider, T., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.032 · Cited by 78 · see citing works
Self-citationLiprin-α3 controls vesicle docking and exocytosis at the active zone of hippocampal synapses
Wong, M. Y., Liu, C., Wang, S. S. H., Roquas, A. C. F., Fowler, S. C., & Kaeser, P. S. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1719012115 · Cited by 77 · see citing works
Self-citationNeurexins cluster Ca2+ channels within the presynaptic active zone
Luo, F., Sclip, A., Jiang, M., & Südhof, T. (2020) · EMBO Journal · doi:10.15252/embj.2019103208 · Cited by 77 · see citing works
Liu, C., Bickford, L. S., Held, R. G., Nyitrai, H., Südhof, T. C., & Kaeser, P. S. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0999-14.2014 · Cited by 73 · see citing works
Self-citationDong, W., Radulović, T., Goral, R. O., Thomas, C. I., Montesinos, M. S., Guerrero‐Given, D., Hagiwara, A., Putzke, T., Hida, Y., Abe, M., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.06.024 · Cited by 70 · see citing works
Held, R. G., Liu, C., & Kaeser, P. S. (2016) · eLife · doi:10.7554/elife.14862 · Cited by 67 · see citing works
Self-citationLAR receptor phospho-tyrosine phosphatases regulate NMDA-receptor responses
Sclip, A., & Südhof, T. C. (2020) · eLife · doi:10.7554/elife.53406 · 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
Self-citationKeller, D. X., Babai, N. Z., Kochubey, O., Han, Y., Markram, H., Schürmann, F., & Schneggenburger, R. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004253 · Cited by 57 · see citing works
Liang, M., Jin, G., Xie, X., Zhang, W., Li, K., Niu, F., Yu, C., & Wei, Z. (2020) · Cell Reports · doi:10.1016/j.celrep.2021.108901 · Cited by 54 · see citing works
RIM-BP2 primes synaptic vesicles via recruitment of Munc13-1 at hippocampal mossy fiber synapses
Brockmann, M. M., Maglione, M., Willmes, C., Stumpf, A., Bouazza, B. A., Velasquez, L. M., Grauel, M., Beed, P., Lehmann, M., Gimber, N., et al. (2018) · bioRxiv · doi:10.7554/elife.43243 · Cited by 53 · see citing works
Brockmann, 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
Zürner, M., & Schoch, S. (2008) · Genomics · doi:10.1016/j.ygeno.2008.10.007 · Cited by 52 · see citing works
Lübbert, M., Goral, R. O., Satterfield, R., Putzke, T., van den Maagdenberg, A. M. J. M., Kamasawa, N., & Young, S. M. (2017) · eLife · doi:10.7554/elife.28412 · Cited by 51 · see citing works
PTPσ Drives Excitatory Presynaptic Assembly via Various Extracellular and Intracellular Mechanisms
Han, K. A., Ko, J. S., Pramanik, G., Kim, J. Y., Tabuchi, K., Um, J. W., & Ko, J. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0672-18.2018 · Cited by 51 · see citing works
Analyses of the spatiotemporal expression and subcellular localization of liprin‐α proteins
Zürner, M., Mittelstaedt, T., Dieck, S. T., Becker, A. J., & Schoch, S. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22664 · Cited by 47 · see citing works
Rebuilding essential active zone functions within a synapse
Tan, C., Wang, S. S. H., de Nola, G., & Kaeser, P. S. (2022) · Neuron · doi:10.1016/j.neuron.2022.01.026 · Cited by 40 · see citing works
Self-citationStructural basis of liprin-α-promoted LAR-RPTP clustering for modulation of phosphatase activity
Xie, X., Luo, L. F., Liang, M., Zhang, W., Zhang, T., Yu, C., & Wei, Z. (2020) · Nature Communications · doi:10.1038/s41467-019-13949-x · Cited by 39 · see citing works
Solution Structure of the RIM1α PDZ Domain in Complex with an ELKS1b C-terminal Peptide
Lu, J., Li, H., Wang, Y., Südhof, T. C., & Rizo, J. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.07.047 · Cited by 38 · see citing works
Liprin-α proteins are master regulators of human presynapse assembly
de la Cruz, B. M., Campos, J., Molinaro, A., Xie, X., Jin, G., Wei, Z., Acuna, C., & Sterky, F. H. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01592-9 · Cited by 32 · see citing works
Intact synapse structure and function after combined knockout of PTPδ, PTPσ, and LAR
Emperador-Melero, J., de Nola, G., & Kaeser, P. S. (2021) · eLife · doi:10.7554/elife.66638 · Cited by 29 · see citing works
Self-citationOh, K. H., Krout, M., Richmond, J. E., & Kim, H. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0076-21.2021 · Cited by 28 · see citing works
Synaptic vesicle capture by CaV2.2 calcium channels
Wong, F. K., Li, Q., & Stanley, E. F. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00101 · Cited by 25 · see citing works
Developmental transformation of Ca2+ channel-vesicle nanotopography at a central GABAergic synapse
Chen, J., Kaufmann, W. A., Chen, C., Arai, I., Kim, O., Shigemoto, R., & Jónás, P. (2024) · Neuron · doi:10.1016/j.neuron.2023.12.002 · Cited by 25 · see citing works
Chen, J., Blanpied, T. A., & Tang, A. (2019) · Methods · doi:10.1016/j.ymeth.2019.07.016 · Cited by 24 · see citing works
Self-citationDifferential nanoscale organization of excitatory synapses onto excitatory vs. inhibitory neurons
Dharmasri, P. A., Levy, A. D., & Blanpied, T. A. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2315379121 · Cited by 23 · see citing works
Self-citationSclip, A., & Südhof, T. C. (2023) · Nature Communications · doi:10.1038/s41467-023-40526-0 · Cited by 22 · see citing works
Rebola, N., Reva, M., Kirizs, T., Szoboszlay, M., Moneron, G., Nusser, Z., & DiGregorio, D. A. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/421370 · Cited by 21 · see citing works
Protein composition of axonal dopamine release sites in the striatum
Kershberg, L., Banerjee, A., & Kaeser, P. S. (2022) · eLife · doi:10.7554/elife.83018 · Cited by 21 · see citing works
Self-citationMetzbower, S. R., Dharmasri, P. A., Levy, A. D., Anderson, M. C., & Blanpied, T. A. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1715-23.2024 · Cited by 19 · see citing works
Self-citationWakita, M., Yamagata, A., Shiroshima, T., Izumi, H., Maeda, A., Sendo, M., Imai, A., Kubota, K., Goto‐Ito, S., Sato, Y., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-14516-5 · Cited by 18 · see citing works
Munc13 supports fusogenicity of non-docked vesicles at synapses with disrupted active zones.
Tan, C., de Nola, G., Qiao, C., Imig, C., Born, R. T., Brose, N., & Kaeser, P. S. (2022) · eLife · doi:10.7554/elife.79077 · Cited by 17 · see citing works
Self-citationCrystal structure of PTPRD phosphatase domain in complex with Liprin-alpha3 tandem SAM domains
Wakita, M., Yamagata, A., & Fukai, S. (2019) · Worldwide Protein Data Bank · doi:10.2210/pdb6kip/pdb · Cited by 12 · see citing works
Liang, M., Jin, G., Xie, X., Zhang, W., Li, K., Niu, F., Yu, C., & Wei, Z. (2020) · SSRN Electronic Journal · doi:10.2139/ssrn.3722054 · Cited by 3 · see citing works
Data table for Emperador-Melero etal 2024
Emperador-Melero, J., & Kaeser, P. S. (2024) · Zenodo (CERN European Organization for Nuclear Research) · doi:10.5281/zenodo.12205516 · Cited by 1 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- [12]Kittel RJ Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 312, 1051– 4 (2006). 16614170
Cited by
Sorted by citations
Trans-synaptic molecular context of NMDA receptor nanodomains
Anderson, M. C., Dharmasri, P. A., Damenti, M., Metzbower, S. R., Laghaei, R., Blanpied, T. A., & Levy, A. D. (2025) · Nature Communications · doi:10.1038/s41467-025-62766-y · Cited by 16 · 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
“The RRP is often equated with the pool of docked vesicles [14] or Munc13 clusters as a proxy of primed vesicles [17,61,76] but also may represent a subpool of primed vesicles [83].”
Bera, M., Grushin, K. S., Sundaram, R. V. K., Hinzen, J. S., Chen, J., Chatterjee, A., Radhakrishnan, A., Lee, S., Padmanarayana, M., Coleman, J., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-62420-7 · Cited by 15 · see citing works
Balancing selectivity and permeability in nanofluidic membranes for osmotic power generation
Han, Q., Peng, P., Liu, Y., Wang, Z. L., & Wei, D. (2025) · Progress in Energy · doi:10.1088/2516-1083/ae0117 · Cited by 14 · see citing works
Phase Separation–Mediated Compartmentalization Underlies Synapse Formation and Plasticity
Wu, X., Shen, Z., & Zhang, M. (2025) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-112723-040159 · Cited by 14 · see citing works
On the targeting of voltage-gated calcium channels to neurotransmitter release sites
Chin, M., & Kaeser, P. S. (2024) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2024.102931 · Cited by 8 · see citing works
Self-citationTuning synapse strength by nanocolumn plasticity
Xu, N., Chen, S.-Y., & Tang, A. (2025) · Trends in Neurosciences · doi:10.1016/j.tins.2024.12.009 · Cited by 10 · see citing works
Chin, M., & Kaeser, P. S. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114428 · Cited by 8 · see citing works
Self-citationMunc13-1 restoration mitigates presynaptic pathology in spinal muscular atrophy
Moradi, M., Weingart, J., Deng, C., Nasouti, M., Briese, M., Jablonka, S., Sauer, M., & Sendtner, M. (2025) · Nature Communications · doi:10.1038/s41467-025-64164-w · Cited by 6 · see citing works
Phase separation in the multi-compartment organization of synapses
Zhu, S., Shen, Z., Wu, X., & Zhang, M. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.102975 · Cited by 7 · see citing works
Status epilepticus alters hippocampal ultrastructure in kainic acid rat model
Zhvania, M. G., Sharikadze, I., Japaridze, N. J., Tizabi, Y., Rzayev, F., Gasimov, E. K., & Lobzhanidze, G. (2025) · Tissue and Cell · doi:10.1016/j.tice.2025.102789 · Cited by 6 · see citing works
Jin, G., Campos, J., Liu, Y., de la Cruz, B. M., Zhang, S., Liang, M., Li, K., Xie, X., Yu, C., Sterky, F. H., et al. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3002817 · Cited by 6 · see citing works
Thivaios, S., Schwenk, J., Bréchet, A., Boudkkazi, S., Sethumadhavan, N., Henneken, P., Miura, E., Hayashi, A., Kocylowski, M. K., Haupt, A., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-77377-4 · Cited by 6 · see citing works
Optical recordings of synaptic vesicle fusion reveal diffusional dispersionPreprint
Lehrich, J., Glyvuk, N., Duan, J., Krishnan, S., Tsytsyura, Y., Keller, U., Sunil, L. P., Nosov, G., Hüve, J., Selenschik, P., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.31.646326 · Cited by 3 · see citing works
Zhao, K., Zhang, L., Lei, M., Jin, Z., Du, T., Zhang, H., Sheng, Y., Hu, Z., Wang, S., & Ma, C. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2508915122 · Cited by 1 · see citing works
CASKIN2 mediates PTPσ-orchestrated transsynaptic mechanisms at excitatory synapses
Han, K. A., Jang, G., Lee, H.-Y., Kim, B., Kanato, T., Vas, V., Buday, L., Liu, X., Choi, S.-Y., Um, J., et al. (2025) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2509116122 · Cited by 2 · see citing works
Active Zone: Linking Resolution Levels of Microscopic Modalities
Galkov, M., Nemcova, P., Dietrich, D., & Schoch, S. (2026) · Advances in neurobiology · doi:10.1007/978-3-032-12594-1_4 · Cited by 1 · see citing works
Synapse formation and plasticity: why is phase separation required?
Zhang, M. (2026) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2026.103193 · Cited by 1 · see citing works
Munc13 serves as a molecular filter for SNARE sorting and assembly in active zone condensates
Zhang, H., Zhang, Y., Zhao, Z., Cao, Z., Zhao, K., Lei, M., Wang, S., & Ma, C. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2529572123 · Cited by 1 · see citing works
The intracellular C-terminus confers compartment-specific targeting of voltage-gated Ca 2+ channelsPreprint
Chin, M., & Kaeser, P. S. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.23.573183
Self-citationEmperador-Melero, J., Signore, S. J. D., González, K. M. D. L., Kaeser, P. S., & Rodal, A. A. (2026) · eLife · doi:10.7554/elife.107276.3
Self-citationEmperador-Melero, J., Signore, S. J. D., González, K. M. D. L., Kaeser, P. S., & Rodal, A. A. (2025) · eLife · doi:10.7554/elife.107276
Self-citationEmperador-Melero, J., Signore, S. J. D., González, K. M. D. L., Kaeser, P. S., & Rodal, A. A. (2025) · eLife · doi:10.7554/elife.107276.1
Self-citationSynaptic active zones are ordered nanostructures designed by supramolecular block copolymersPreprint
Sakamoto, H., & Shimobayashi, S. F. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.15.691964
Padmanabhan, N., Twilley, R. E., Oku, S., Rabbi, M. S., Skeens, A., Jones, G. C., Acharya, S., Basha, M. A., Rajapakse, D., Koltek, C., et al. (2026) · Neuron · doi:10.1016/j.neuron.2026.06.018
Voorn, R. A., Sternbach, M., Bourien, J., Komiyama, N. H., Rankovic, V., Wolf, F., Grant, S. G. N., & Vogl, C. (2026) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2026.1866692
Engineered proteins to restore and enhance neurotransmitter releasePreprint
Chin, M., Yang, K., Ricardo López, C., Tan, C., & Kaeser, P. S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.10.23.761409
Self-citation
- Authors
- Emperador-Melero, J., Andersen, J. W., Metzbower, S. R., Levy, A. D., Dharmasri, P. A., de Nola, G., Blanpied, T. A., & Kaeser, P. S.
- Affiliations
- Harvard University (US)
- University of Maryland, Baltimore (US)
- Corresponding author
- Kaeser, Pascal S.
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2024-08-19
- Volume
- 27
- Issue
- 9
- Pages
- 1680-1694
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC11682530
- OpenAlex
- W4401685161
- Cited by
- 27
- References
- 89
- Citations by year
- 2026: 8 · 2025: 15 · 2024: 3 · 2023: 1
- FWCI
- 4.55
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (R01NS083898, K99NS129959)
- U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (R01MH113349, F31MH117920, R37MH080046)
- Harvard Medical School (NA)
- 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 › Ion channel regulation and function
- Keywords
- active zone, synaptic vesicle priming, Munc13, RIM, Liprin-α, PTPσ, hippocampal synapses, neurotransmitter release
- MeSH terms
- Animals, Hippocampus, Mice, Inbred C57BL, Nerve Tissue Proteins, Synapses, Synaptic Vesicles, Calcium Channels, Mice, Knockout, Caveolin 2, 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