RIM genes differentially contribute to organizing presynaptic release sites
Open accessAbstract
Tight coupling of Ca(2+) channels to the presynaptic active zone is critical for fast synchronous neurotransmitter release. RIMs are multidomain proteins that tether Ca(2+) channels to active zones, dock and prime synaptic vesicles for release, and mediate presynaptic plasticity. Here, we use conditional knockout mice targeting all RIM isoforms expressed by the Rims1 and Rims2 genes to examine the contributions and mechanism of action of different RIMs in neurotransmitter release. We show that acute single deletions of each Rims gene decreased release and impaired vesicle priming but did not alter the extracellular Ca(2+)-responsiveness of release (which for Rims gene mutants is a measure of presynaptic Ca(2+) influx). Moreover, single deletions did not affect the synchronization of release (which depends on the close proximity of Ca(2+) channels to release sites). In contrast, deletion of both Rims genes severely impaired the Ca(2+) responsiveness and synchronization of release. RIM proteins may act on Ca(2+) channels in two modes: They tether Ca(2+) channels to active zones, and they directly modulate Ca(2+)-channel inactivation. The first mechanism is essential for localizing presynaptic Ca(2+) influx to nerve terminals, but the role of the second mechanism remains unknown. Strikingly, we find that although the RIM2 C(2)B domain by itself significantly decreased Ca(2+)-channel inactivation in transfected HEK293 cells, it did not rescue any aspect of the RIM knockout phenotype in cultured neurons. Thus, RIMs primarily act in release as physical Ca(2+)-channel tethers and not as Ca(2+)-channel modulators. Different RIM proteins compensate for each other in recruiting Ca(2+) channels to active zones, but contribute independently and incrementally to vesicle priming.
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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 [74]
The Abstract says RIMs bind other active-zone components and participate in neurotransmitter release. The Results say RIM1 and RIM2 promote vesicle priming through Munc13, but our copy does not say they recruit Munc13-1 to active zones specifically. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThis difference might result from direct, fixed-length interaction between the PZD domain of RIM1/2 and the CaV2.1 C-terminus, which is difficult to modulate.
“This might result from direct, fixed-length interaction between the PZD domain of RIM1/2 and the CaV2.1 C-terminus [73,74], which is difficult to modulate.”
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 [74]
The Abstract states that RIM PDZ domains directly bind the C-termini of P/Q-type Ca2+ channels, supporting the proposed interaction with CaV2.1. Neither the Abstract nor the Discussion describes that interaction as fixed-length or difficult to modulate. (LLM, conf=0.88)
Experimental — accuracy not yet measured
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Cites
Definition of the readily releasable pool of vesicles at hippocampal synapses.
Rosenmund, C., & Stevens, C. (1996) · Neuron · doi:10.1016/s0896-6273(00)80146-4 · Cited by 1,084 · see citing works
Synaptotagmin I functions as a calcium regulator of release probability
Fernández-Chacón, R., Königstorfer, A., Gerber, S. H., García, J., Matos, M. F., Stevens, C. F., Brose, N., Rizo, J., Rosenmund, C., & Südhof, T. C. (2001) · Nature · doi:10.1038/35065004 · Cited by 961 · see citing works
Self-citationRim 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
Self-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
Self-citationFunctional 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
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-citationRIM 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-citationA post-docking role for active zone protein Rim
Koushika, S. P., Richmond, J. E., Hadwiger, G., Weimer, R. M., Jørgensen, E. M., & Nonet, M. L. (2001) · Nature Neuroscience · doi:10.1038/nn732 · Cited by 320 · 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-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
Conformational switch of syntaxin-1 controls synaptic vesicle fusion
Gerber, S. H., Rah, J.-C., Min, S.-W., Liu, X., de Wit, H., Dulubova, I., Meyer, A. C., Rizo, J., Arancillo, M., Hammer, R. E., et al. (2008) · Science · doi:10.1126/science.1163174 · Cited by 294 · see citing works
Self-citationLiprins, 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
Self-citationRIM 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
Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1α
Chevaleyre, V., Heifets, B. D., Kaeser, P. S., Südhof, T. C., & Castillo, P. E. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.020 · Cited by 261 · see citing works
Self-citationWang, 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
Self-citationThe RIM/NIM Family of Neuronal C2 Domain Proteins
Wang, Y., Sugita, S., & Südhof, T. C. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m909008199 · Cited by 243 · see citing works
Self-citationMaximov, A., & Südhof, T. C. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.006 · Cited by 238 · see citing works
Self-citationPang, Z. P., Melicoff, E., Padgett, D., Liu, Y., Teich, A. F., Dickey, B. F., Lin, W., Adachi, R., & Südhof, T. C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3519-06.2006 · Cited by 228 · see citing works
Self-citationSCRAPPER-Dependent Ubiquitination of Active Zone Protein RIM1 Regulates Synaptic Vesicle Release
Yao, I., Takagi, H., Ageta, H., Kahyo, T., Sato, S., Hatanaka, K., Fukuda, Y., Chiba, T., Morone, N., Yuasa, S., et al. (2007) · Cell · doi:10.1016/j.cell.2007.06.052 · Cited by 200 · see citing works
Distinct Rab Binding Specificity of Rim1, Rim2, Rabphilin, and Noc2
Fukuda, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m212341200 · Cited by 189 · see citing works
UNC-13 and UNC-10/Rim Localize Synaptic Vesicles to Specific Membrane Domains
Weimer, R., Gracheva, E. O., Meyrignac, O., Miller, K. G., Richmond, J., & Bessereau, J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2350-06.2006 · Cited by 169 · see citing works
Monitoring synaptic transmission in primary neuronal cultures using local extracellular stimulation
Maximov, A., Pang, Z. P., Tervo, D. G. R., & Südhof, T. C. (2006) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2006.10.009 · Cited by 138 · see citing works
Self-citationMolecular organization and plasticity of the cytomatrix at the active zone
Gundelfinger, E. D., & Fejtová, A. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.10.005 · Cited by 133 · see citing works
Structural Basis for a Munc13–1 Homodimer to Munc13–1/RIM Heterodimer Switch
Lu, J., Machius, M., Dulubova, I., Dai, H., Südhof, T. C., Tomchick, D. R., & Rizo, J. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040192 · Cited by 132 · 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-citationWang, Y., & Südhof, T. C. (2003) · Genomics · doi:10.1016/s0888-7543(02)00024-1 · Cited by 112 · see citing works
Self-citationcAMP/PKA signaling and RIM1α mediate presynaptic LTP in the lateral amygdala
Fourcaudot, E., Gambino, F., Humeau, Y., Casassus, G., Shaban, H., Poulain, B., & Lüthi, A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806938105 · Cited by 105 · see citing works
ELKS2α/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-citationHo, A., Morishita, W., Atasoy, D., Liu, X., Tabuchi, K., Hammer, R. E., Malenka, R. C., & Südhof, T. C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2855-06.2006 · Cited by 100 · 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-citationKaeser, P. S., Kwon, H.-B., Blundell, J., Chevaleyre, V., Morishita, W., Malenka, R. C., Powell, C. M., Castillo, P. E., & Südhof, T. C. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806679105 · Cited by 74 · see citing works
Self-citationAdapter protein 14-3-3 is required for a presynaptic form of LTP in the cerebellum
Simsek‐Duran, F., Linden, D. J., & Lónárt, G. (2004) · Nature Neuroscience · doi:10.1038/nn1348 · Cited by 53 · see citing works
Uriu, Y., Kiyonaka, S., Miki, T., Yagi, M., Akiyama, S., Mori, E., Nakao, A., Beedle, A. M., Campbell, K. P., Wakamori, M., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.101311 · Cited by 46 · 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
Pushing synaptic vesicles over the RIM
Kaeser, P. S. (2011) · Cellular Logistics · doi:10.4161/cl.1.3.16429 · Cited by 21 · see citing works
Self-citationGracheva, E. O., Hadwiger, G., Nonet, M., & Richmond, J. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.08.026 · Cited by 1 · see citing works
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ICGC PedBrain-Seq Project, Gröbner, S. N., ICGC MMML-Seq Project, Worst, B. C., Weischenfeldt, J., Buchhalter, I., Kleinheinz, K., Rudneva, V. A., Johann, P. D., Balasubramanian, G. P., et al. (2018) · Nature · doi:10.1038/nature25480 · Cited by 1,572 · see citing works
Neurotransmitter Release: The Last Millisecond in the Life of a Synaptic Vesicle
Südhof, T. C. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.022 · Cited by 1,197 · see citing works
Self-citationSüdhof, T. C. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.012 · Cited by 1,062 · see citing works
Self-citationMolecular Mechanisms for Synchronous, Asynchronous, and Spontaneous Neurotransmitter Release
Kaeser, P. S., & Regehr, W. G. (2014) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021113-170338 · Cited by 447 · see citing works
Self-citationCircRNA accumulation in the aging mouse brain
Gruner, H. N., Cortés-López, M., Cooper, D. A., Bauer, M. J., & Miura, P. (2016) · Scientific Reports · doi:10.1038/srep38907 · Cited by 366 · see citing works
Synaptic vesicle recycling: steps and principles
Rizzoli, S. O. (2014) · The EMBO Journal · doi:10.1002/embj.201386357 · Cited by 317 · see citing works
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Földy, C., Malenka, R. C., & Südhof, T. C. (2013) · Neuron · doi:10.1016/j.neuron.2013.02.036 · Cited by 287 · see citing works
Self-citationPresynaptic calcium channels: specialized control of synaptic neurotransmitter release
DOLPHIN, A. C., & Lee, A. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0278-2 · Cited by 274 · see citing works
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Otero-Garcia, M., Mahajani, S. U., Wakhloo, D., Tang, W., Xue, Y.-Q., Morabito, S., Pan, J., Oberhauser, J., Madira, A. E., Shakouri, T., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.06.021 · Cited by 262 · see citing works
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Gundelfinger, E. D., Reissner, C., & Garner, C. C. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2015.00019 · Cited by 203 · see citing works
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Wu, H., Yin, Q.-F., Luo, Z., Yao, R.-W., Zheng, C.-C., Zhang, J., Xiang, J., Yang, L. C., & Chen, L. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.10.007 · Cited by 154 · see citing works
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Self-citationCzéh, B., Vardya, I., Varga, Z., Febbraro, F., Csabai, D., Martis, L., Højgaard, K., Henningsen, K., Bouzinova, E. V., Miseta, A., et al. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00148 · Cited by 129 · see citing works
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Crosby, K. C., Gookin, S. E., Garcia, J. D., Zent, K. H., Dell’Acqua, M. L., & Smith, K. R. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.02.070 · Cited by 126 · see citing works
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Emerging Synaptic Molecules as Candidates in the Etiology of Neurological Disorders
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Processing and roles of snoRNA-ended long noncoding RNAs
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Cárdenas, A. M., & Marengo, F. D. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13565 · Cited by 32 · see citing works
He, R., Zhang, J., Yu, Y., Jizi, L., Wang, W.-Z., & Li, M.-L. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00213 · Cited by 32 · see citing works
Ohara‐Imaizumi, M., Aoyagi, K., Yamauchi, H., Yoshida, M., Mori, M. X., Hida, Y., Tran, H. N., Ohkura, M., Abe, M., Akimoto, Y., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2018.12.106 · Cited by 32 · see citing works
Liau, W., Samaddar, S., Banerjee, S., & Bredy, T. W. (2021) · RNA Biology · doi:10.1080/15476286.2020.1868165 · Cited by 27 · see citing works
Presynaptic [Ca2+] and GCAPs: aspects on the structure and function of photoreceptor ribbon synapses
Schmitz, F. (2014) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2014.00003 · Cited by 31 · see citing works
Structure of the neuromuscular junction: function and cooperative mechanisms in the synapse
Takamori, M. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06784.x · Cited by 31 · see citing works
Analysis of RIM Expression and Function at Mouse Photoreceptor Ribbon Synapses
Löhner, M., Babai, N. Z., Müller, T. M., Gierke, K., Atorf, J., Joachimsthaler, A., Peukert, A., Martens, H., Feigenspan, A., Kremers, J., et al. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2795-16.2017 · Cited by 31 · see citing works
Active zones of mammalian neuromuscular junctions: formation, density, and aging
Nishimune, H. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06836.x · Cited by 31 · see citing works
Upsetting the Balance: When Viruses Manipulate Cell Polarity Control
Thomas, M., & Banks, L. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.04.016 · Cited by 30 · see citing works
High-throughput sequencing of the synaptome in major depressive disorder
Pirooznia, M., Wang, T., Avramopoulos, D., Potash, J. B., Zandi, P. P., & Goes, F. S. (2015) · Molecular Psychiatry · doi:10.1038/mp.2015.98 · Cited by 29 · see citing works
Zhao, H., Du, H., Liu, M., Gao, S., Li, N., Chao, Y., Li, R., Chen, W., Lou, Z., & Dong, X. (2017) · Journal of Proteome Research · doi:10.1021/acs.jproteome.7b00724 · Cited by 29 · see citing works
Genome-Wide Detection of Copy Number Variations in Unsolved Inherited Retinal Disease
Huang, X., Mao, J.-Y., Huang, Z., Rao, F.-Q., Cheng, F., Li, F., Wang, Q., & Jin, Z. (2017) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.16-20705 · Cited by 27 · see citing works
Carbajo‐García, M. C., Corachán, A., Juárez‐Barber, E., Monleón, J., Payá, V., Trelis, A., Quiñonero, A., Pellicer, A., & Ferrero, H. (2022) · The Journal of Pathology · doi:10.1002/path.5920 · Cited by 27 · see citing works
Neuronal hibernation following hippocampal demyelination
Baltan, S., Jawaid, S., Chomyk, A. M., Kidd, G. J., Chen, J. M., Battapady, H. D., Chan, R., Dutta, R., & Trapp, B. D. (2021) · Acta Neuropathologica Communications · doi:10.1186/s40478-021-01130-9 · Cited by 25 · see citing works
Orvis, J., Albertin, C. B., Shrestha, P., Chen, S., Zheng, M., Rodriguez, C. J., Tallon, L. J., Mahurkar, A., Zimin, A. V., Kim, M., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2122301119 · Cited by 26 · 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
Circular RNAs constitute an inherent gene regulatory axis in the mammalian eye and brain
George, A. K., Master, K., Majumder, A., Homme, R. P., Laha, A., Sandhu, H. S., Tyagi, S. C., & Singh, M. (2018) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2018-0505 · Cited by 24 · see citing works
Wu, S., Fan, J., Tang, F., Chen, L., Zhang, X., Xiao, D., & Li, X. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1123561 · Cited by 24 · see citing works
Gómez‐Varela, D., & Berg, D. K. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1482-13.2013 · Cited by 23 · see citing works
Vo, V. T. A., Kim, S., Hua, T. N. M., Oh, J., & Jeong, Y. (2022) · Communications Biology · doi:10.1038/s42003-022-03538-y · Cited by 22 · see citing works
Nanomachinery Organizing Release at Neuronal and Ribbon Synapses
Chakrabarti, R., & Wichmann, C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092147 · Cited by 22 · see citing works
Jackson, T. C., & Kochanek, P. M. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00126 · Cited by 20 · see citing works
DNA methylation clocks for clawed frogs reveal evolutionary conservation of epigenetic aging
Zoller, J. A., Parasyraki, E., Lu, A. T.-H., Haghani, A., Niehrs, C., & Horvath, S. (2023) · GeroScience · doi:10.1007/s11357-023-00840-3 · Cited by 22 · see citing works
Synaptotagmin-1 is a Ca2+ sensor for somatodendritic dopamine release
Lebowitz, J. J., Banerjee, A., Qiao, C., Bunzow, J. R., Williams, J. T., & Kaeser, P. S. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111915 · Cited by 19 · see citing works
Self-citationParoxysmal movement disorders: Paroxysmal dyskinesia and episodic ataxia
Erro, R., Magrinelli, F., & Bhatia, K. P. (2023) · Handbook of clinical neurology · doi:10.1016/b978-0-323-98817-9.00033-8 · Cited by 19 · see citing works
Devyatkin, V. A., Redina, O. E., Kolosova, N. G., & Muraleva, N. A. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-190956 · Cited by 19 · see citing works
Ghasemi, D. R., Okonechnikov, K., Rademacher, A., Tirier, S. M., Maaß, K. K., Schumacher, H., Joshi, P. K., Gold, M. P., Sundheimer, J. K., Statz, B., et al. (2024) · Nature Communications · doi:10.1038/s41467-023-44117-x · Cited by 18 · see citing works
Fast, Ca2+-dependent exocytosis at nerve terminals: Shortcomings of SNARE-based models
Meriney, S. D., Umbach, J. A., & Gundersen, C. B. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.07.001 · Cited by 17 · 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-citationGene networks associated with non-syndromic intellectual disability
Lee, S., Rudd, S. A., Gratten, J., Visscher, P. M., Prins, J. B., & Dawson, P. A. (2017) · Journal of Neurogenetics · doi:10.1080/01677063.2017.1404058 · Cited by 16 · see citing works
Kim, 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
“This might result from direct, fixed-length interaction between the PZD domain of RIM1/2 and the Ca V 2.1 C-terminus [73,74], which is difficult to modulate.”
InfluentialUltrastructural analysis of wild-type and RIM1α knockout active zones in a large cortical synapse
Lichter, K., Paul, M. M., Pauli, M., Schoch, S., Kollmannsberger, P., Stigloher, C., Heckmann, M., & Sirén, A.-L. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111382 · Cited by 15 · see citing works
Similarity and Diversity of Presynaptic Molecules at Neuromuscular Junctions and Central Synapses
Takikawa, K., & Nishimune, H. (2022) · Biomolecules · doi:10.3390/biom12020179 · Cited by 18 · see citing works
Honeybee gut microbiota modulates host behaviors and neurological processesPreprint
Zhang, Z., Mu, X., Cao, Q., Shi, Y., Hu, X., & Zheng, H. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.19.423587 · Cited by 15 · see citing works
Jackson, R. E., & Burrone, J. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00021 · Cited by 14 · see citing works
Identification of Novel Targets of RBM5 in the Healthy and Injured Brain
Jackson, T. C., Janesko‐Feldman, K. L., Gorse, K., Vagni, V., Jackson, E. K., & Kochanek, P. M. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.04.024 · Cited by 13 · see citing works
MicroRNA Alteration in Developing Rat Oligodendrocyte Precursor Cells Induced by Hypoxia-Ischemia
Su, X., Xiao, D., Huang, L., Li, S., Ying, J., Yu, T., Ye, Q., Mu, D., & Qu, Y. (2019) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlz071 · Cited by 13 · see citing works
Episodic and Electrical Nervous System Disorders Caused by Nonchannel Genes
Lee, H.-Y., Fu, Y., & Ptáček, L. J. (2014) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021014-071814 · Cited by 12 · see citing works
The 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
Milet, J., Sabbagh, A., Migot‐Nabias, F., Luty, A. J. F., Gaye, O., Garcia, A., & Courtin, D. (2016) · Genes and Immunity · doi:10.1038/gene.2015.59 · Cited by 11 · see citing works
New insights into tardive dyskinesia genetics: Implementation of whole-exome sequencing approach
Alkelai, A., Greenbaum, L., Heinzen, E. L., Baugh, E. H., Teitelbaum, A., Zhu, X., Strous, R. D., Tatarskyy, P., Zai, C. C. H., Tiwari, A. K., et al. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109659 · Cited by 10 · see citing works
Outside‐in regulation of the readily releasable pool of synaptic vesicles by α2δ‐1
Segundo, P. M. S., Terni, B., Burgueño, J., Monroy, X., Dordal, A., Merlos, M., & Llobet, A. (2019) · The FASEB Journal · doi:10.1096/fj.201901551r · Cited by 10 · see citing works
Li, X., Cai, D., Huang, Y., Xie, Y., Shen, D., Yuan, Z., Liu, X., Huang, M., Luo, Y., Yu, H., et al. (2023) · BMC Cancer · doi:10.1186/s12885-023-10765-x · Cited by 10 · see citing works
Piekut, T., Wong, Y. Y., Walker, S. E., Smith, C. L., Gauberg, J., Harracksingh, A. N., Lowden, C., Novogradac, B. B., Cheng, H. M., Spencer, G. E., et al. (2020) · Genome Biology and Evolution · doi:10.1093/gbe/evaa097 · Cited by 10 · see citing works
Cortical development dynamics across autism spectrum disorder mouse models
Schwarz, L. A., Dotter, C. P., Isaev, S. V., Lisi, M., Malzl, D., Bueschl, C., Ladstätter, S., Oliveira, B., Barel, M., Basilico, B., et al. (2026) · Nature · doi:10.1038/s41586-026-10679-1 · Cited by 10 · see citing works
How Do RIM-BPs Link Voltage-Gated Ca 2+ Channels to Evoked Neurotransmitter Release?
Li, Y. C., & Kavalali, E. T. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.005 · Cited by 7 · see citing works
Magrinelli, F., & Bhatia, K. P. (2024) · Handbook of clinical neurology · doi:10.1016/b978-0-323-90820-7.00010-0 · Cited by 6 · see citing works
Crawford, D. C., Jiang, X., Taylor, A., Moulder, K. L., & Mennerick, S. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051930 · Cited by 6 · see citing works
Nanoscaled RIM clustering at presynaptic active zones revealed by endogenous tagging
Mrestani, A., Dannhäuser, S., Pauli, M., Kollmannsberger, P., Hübsch, M., Morris, L., Langenhan, T., Heckmann, M., & Paul, M. M. (2023) · Life Science Alliance · doi:10.26508/lsa.202302021 · Cited by 6 · see citing works
Lerebours, A., Chapman, E., Lyons, B. P., Bignell, J. P., Stentiford, G. D., & Rotchell, J. M. (2017) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2017.04.052 · Cited by 6 · see citing works
Spinal cord injury regulates circular RNA expression in axons
Siddiq, M. M., Toro, C. A., Johnson, N. P., Hansen, J., Xiong, Y., Mellado, W., Tolentino, R. E., Johnson, K., Jayaraman, G., Suhail, Z., et al. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1183315 · Cited by 6 · see citing works
Laighneach, A., Kelly, J., Desbonnet, L., Holleran, L., Kerr, D., McKernan, D., Donohoe, G., & Morris, D. W. (2023) · bioRxiv · doi:10.1371/journal.pone.0295855 · Cited by 5 · see citing works
Physiological Expression of Ion Channel Receptors in Human Periodontal Ligament Stem Cells
Chiricosta, L., Diomede, F., Trubiani, O., Bramanti, P., & Mazzon, E. (2019) · Cells · doi:10.3390/cells8030219 · Cited by 4 · see citing works
Developmental emergence of cortical neurogliaform cell diversity
Gomez, L., Cadilhac, C., Prados, J., Mule, N., Jabaudon, D., & Dayer, A. G. (2023) · Development · doi:10.1242/dev.201830 · Cited by 4 · see citing works
DNA methylation clocks for clawed frogs reveal evolutionary conservation of epigenetic ageingPreprint
Zoller, J. A., Parasyraki, E., Lu, A. T.-H., Haghani, A., Niehrs, C., & Horvath, S. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.02.502561 · Cited by 4 · see citing works
Farooq, J., Snyder, K. L., Janesko‐Feldman, K. L., Gorse, K., Vagni, V., Kochanek, P. M., & Jackson, T. C. (2022) · Journal of Neurotrauma · doi:10.1089/neu.2021.0362 · Cited by 3 · see citing works
Der molekulare Mechanismus der Neurotransmitterfreisetzung und Nervenzell-Synapsen (Nobel-Aufsatz)†
Südhof, T. (2014) · Angewandte Chemie · doi:10.1002/ange.201406359 · Cited by 2 · see citing works
Self-citationMolecular and Morphological Correlates of Synaptic Vesicle Priming
Imig, C. (2014) · doi:10.53846/goediss-4755 · Cited by 3 · see citing works
Modeling Synaptic Maturation From Growth Cone to Synapse in Human Organoids
Øhlenschlæger, M. S., Criscuolo, L., Jensen, P., Sanchez, D. J. L.-D., Sutcliffe, M. A., Bhosale, S., Bogetofte, H., Tahir, M., Jakobsen, L. A., Pihl, M., et al. (2026) · Journal of Neurochemistry · doi:10.1111/jnc.70458 · Cited by 3 · see citing works
La machinerie moléculaire de sécrétion des neurotransmetteurs
Südhof, T. (2015) · Biologie Aujourd hui · doi:10.1051/jbio/2015012 · Cited by 1 · see citing works
Self-citation
- Authors
- Kaeser, P. S., Deng, L., Fan, M., & Südhof, T. C.
- Affiliations
- Howard Hughes Medical Institute (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-07-02
- Volume
- 109
- Issue
- 29
- Pages
- 11830-11835
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3406861
- OpenAlex
- W2029142270
- Cited by
- 115
- References
- 39
- Citations by year
- 2026: 6 · 2025: 2 · 2024: 6 · 2023: 11 · 2022: 11 · 2021: 4 · 2020: 10 · 2019: 10 · 2018: 9 · 2017: 10 · 2016: 8 · 2015: 4 · 2014: 10 · 2013: 10 · 2012: 4
- FWCI
- 3.69
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- U.S. Public Health Service (P0MH086403)
- National Institute on Drug Abuse (DA029044, K01DA029044)
- National Institute of Neurological Disorders and Stroke (R01NS077906)
- 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, neurotransmitter release, calcium channel inactivation, presynaptic calcium influx, conditional knockout mice, C2B domain
- MeSH terms
- Animals, Calcium, Evoked Potentials, Hippocampus, Humans, Lipids, Calcium Channels, Presynaptic Terminals, Mice, Knockout, Patch-Clamp Techniques, GTP-Binding Proteins, rab3 GTP-Binding Proteins, Mice, HEK293 Cells
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