Redundant Localization Mechanisms of RIM and ELKS in Caenorhabditis elegans
Open accessAbstract
Active zone proteins play a fundamental role in regulating neurotransmitter release and defining release sites. The functional roles of active zone components are beginning to be elucidated; however, the mechanisms of active zone protein localization are unknown. Studies have shown that glutamine, leucine, lysine, and serine-rich protein (ELKS), a recently defined member of the active zone complex, acts to localize the active zone protein Rab3a-interacting molecule (RIM) and regulates synaptic transmission in cultured neurons. Here, we test the function of ELKS in vivo. Like mammalian ELKS, Caenorhabditis elegans ELKS is an active zone protein that directly interacts with the postsynaptic density-25/Discs large/zona occludens (PDZ) domain of RIM. However, RIM protein localizes in the absence of ELKS and vice versa. In addition, elks mutants exhibit neither the behavioral nor the physiological defects associated with unc-10 RIM mutants, indicating that ELKS is not a critical component of the C. elegans release machinery. Interestingly, expression of the soluble PDZ domain of RIM disrupts ELKS active zone targeting, suggesting a tight association between the two proteins in vivo. RIM truncations containing only the PDZ and C2A domains target to release sites in an ELKS-dependent manner. Together, these data identify ELKS as a new member of the C. elegans active zone complex, define the role of ELKS in synaptic transmission, and characterize the relationship between ELKS and RIM in vivo. Furthermore, they demonstrate that multiple different protein-protein interactions redundantly anchor both ELKS and RIM to active zones and implicate novel proteins in the formation of the active zone.
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?
Deletion of ELKS in C. elegans and of ELKS2 in mice did not impair neurotransmitter release.
“deletion of ELKS in C. elegans and of ELKS2 in mice did not impair neurotransmitter release (Deken et al., 2005; Kaeser et al., 2009).”
From The Presynaptic Active Zone (2012) · cites this paper as Deken et al., 2005
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
Molecular Cloning: A Laboratory Manual
Sambrook, J., Fritsch, E., & Maniatis, T. (1989) · UCLA - Biblioteca de Ciencias de la Salud · Cited by 133,589 · see citing works
NF-κB regulation in the immune system
Li, Q., & Verma, I. M. (2002) · Nature Reviews Immunology · doi:10.1038/nri910 · Cited by 4,007 · see citing works
Mello, C. C., Kramer, J. M., Stinchcomb, D. T., & Ambros, V. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb04966.x · Cited by 3,069 · see citing works
The Nematode Caenorhabditis elegans
Wood, W. B. (1988) · Cold Spring Harbor Laboratory eBooks · Cited by 2,821 · see citing works
Südhof, T. C. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131412 · Cited by 2,491 · 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
NF-κB functions in synaptic signaling and behavior
Meffert, M. K., Chang, J. M., Wiltgen, B. J., Fanselow, M. S., & Baltimore, D. (2003) · Nature Neuroscience · doi:10.1038/nn1110 · Cited by 690 · 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
UNC-13 is required for synaptic vesicle fusion in C. elegans
Richmond, J. E., Davis, W. S., & Jørgensen, E. M. (1999) · Nature Neuroscience · doi:10.1038/14755 · Cited by 617 · see citing works
Assembly of presynaptic active zones from cytoplasmic transport packets
Ahmari, S. E., Buchanan, J., & Smith, S. J. (2000) · Nature Neuroscience · doi:10.1038/74814 · Cited by 596 · 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
Phillips, G. R., Huang, J. K., Wang, Y., Tanaka, H., Shapiro, L. S., Zhang, W., Shan, W., Arndt, K., Frank, M., Gordon, R. E., et al. (2001) · Neuron · doi:10.1016/s0896-6273(01)00450-0 · Cited by 438 · see citing works
A genetic selection for Caenorhabditis elegans synaptic transmission mutants.
Miller, K. G., Alfonso, A., Nguyen, M., Crowell, J. A., Johnson, C. D., & Rand, J. B. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.22.12593 · Cited by 437 · 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
Assembling the Presynaptic Active Zone
Zhai, R. G., Vardinon-Friedman, H., Cases-Langhoff, C., Becker, B., Gundelfinger, E. D., Ziv, N. E., & Garner, C. C. (2001) · Neuron · doi:10.1016/s0896-6273(01)00185-4 · Cited by 424 · 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
The 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
Nonet, M. L., Staunton, J. E., Kilgard, M. P., Fergestad, T., Hartwieg, E. A., Horvitz, H. R., Jørgensen, E. M., & Meyer, B. J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08061.1997 · Cited by 354 · see citing works
Self-citationDrosophila Unc-13 is essential for synaptic transmission
Aravamudan, B., Fergestad, T., Davis, W. S., Rodesch, C. K., & Broadie, K. S. (1999) · Nature Neuroscience · doi:10.1038/14764 · Cited by 335 · see citing works
A 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
Self-citationCellular and molecular mechanisms of presynaptic assembly
Ziv, N. E., & Garner, C. C. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1370 · Cited by 306 · see citing works
The Taxonomy of Developmental Control in <i>Caenorhabditis elegans</i>
Ruvkun, G., & Hobert, O. (1998) · Science · doi:10.1126/science.282.5396.2033 · Cited by 305 · see citing works
Ohtsuka, T., Takao‐Rikitsu, E., Inoue, E., Inoue, M., Takeuchi, M., Matsubara, K., Deguchi‐Tawarada, M., Satoh, K., Morimoto, K., Nakanishi, H., et al. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200202083 · Cited by 295 · see citing works
The Architecture of the Active Zone in the Presynaptic Nerve Terminal
Zhai, R. G., & Bellen, H. J. (2004) · Physiology · doi:10.1152/physiol.00014.2004 · Cited by 291 · see citing works
Synaptic Transmission Deficits inCaenorhabditis elegansSynaptobrevin Mutants
Nonet, M. L., Saifee, O., Zhao, H., Rand, J. B., & Wei, L. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00070.1998 · Cited by 283 · see citing works
Self-citationNonet, M. L., Holgado, A. M., Brewer, F., Serpe, C. J., Norbeck, B. A., Holleran, J. L., Wei, L., Hartwieg, E. A., Jørgensen, E. M., & Alfonso, A. (1999) · Molecular Biology of the Cell · doi:10.1091/mbc.10.7.2343 · Cited by 272 · see citing works
Self-citationAltrock, W. D., tom Dieck, S., Sokolov, M., Meyer, A. C., Sigler, A., Brakebusch, C., Fässler, R., Richter, K., Boeckers, T. M., Potschka, H., et al. (2003) · Neuron · doi:10.1016/s0896-6273(03)00088-6 · Cited by 258 · 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
Wang, Z.-W., Saifee, O., Nonet, M. L., & Salkoff, L. (2001) · Neuron · doi:10.1016/s0896-6273(01)00522-0 · Cited by 231 · see citing works
Self-citationTakao-Rikitsu, E., Mochida, S., Inoue, E., Deguchi-Tawarada, M., Inoue, M., Ohtsuka, T., & Takai, Y. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200307101 · Cited by 221 · see citing works
Activation of Transcription Factor NF-κB Requires ELKS, an IκB Kinase Regulatory Subunit
Sigala, J. L. D., Bottero, V., Young, D. B., Shevchenko, A., Mercurio, F., & Verma, I. M. (2004) · Science · doi:10.1126/science.1098387 · Cited by 220 · see citing works
The presynaptic cytomatrix of brain synapses
Dresbach, T., Qualmann, B., Kessels, M. M., Garner, C. C., & Gundelfinger, E. D. (2001) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000781 · Cited by 216 · 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
High-Throughput Isolation of Caenorhabditis elegans Deletion MutantsPreprint
Liu, L. X., Spoerke, J. M., Mulligan, E. L., Chen, J., Reardon, B., Westlund, B., Sun, L., Abel, K., Armstrong, B. A., Hardiman, G., et al. (1999) · Genome Research · doi:10.1101/gr.9.9.859 · Cited by 175 · see citing works
Characterization of novel Rab6-interacting proteins involved in endosome-to-TGN transport
Monier, S., Jollivet, F., Janoueix‐Lerosey, I., Johannes, L., & Goud, B. (2002) · Traffic · doi:10.1034/j.1600-0854.2002.030406.x · Cited by 170 · see citing works
Transport rates of GABA transporters: regulation by the N-terminal domain and syntaxin 1A
Deken, S. L., Beckman, M. L., Boos, L., & Quick, M. W. (2000) · Nature Neuroscience · doi:10.1038/79939 · Cited by 158 · see citing works
Self-citationMultiple Roles for the Active Zone Protein RIM1α in Late Stages of Neurotransmitter Release
Calakos, N., Schoch, S., Südhof, T. C., & Malenka, R. C. (2004) · Neuron · doi:10.1016/j.neuron.2004.05.014 · Cited by 150 · see citing works
Molecular mechanisms of active zone function
Rosenmund, C., Rettig, J., & Brose, N. (2003) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2003.09.011 · 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
Nakata, T., Kitamura, Y., Shimizu, K., Tanaka, S., Fujimori, M., Yokoyama, S., Ito, K., & Emi, M. (1999) · Genes Chromosomes and Cancer · doi:10.1002/(sici)1098-2264(199906)25:2 · Cited by 133 · see citing works
The synaptic vesicle cycle: exocytosis and endocytosis in Drosophila and C. elegans
Richmond, J. E., & Broadie, K. S. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00360-4 · Cited by 112 · see citing works
Wang, Y., & Südhof, T. C. (2003) · Genomics · doi:10.1016/s0888-7543(02)00024-1 · Cited by 112 · see citing works
Johnson, S., Halford, S., Morris, A. G., Patel, R. J., Wilkie, S. E., Hardcastle, A. J., Moore, A. T., Zhang, K., & Hunt, D. M. (2003) · Genomics · doi:10.1016/s0888-7543(03)00010-7 · Cited by 101 · see citing works
Expression of multiple UNC-13 proteins in the Caenorhabditis elegans nervous system.
Kohn, R., Duerr, J., McManus, J. R., Duke, A., Rakow, T. L., Maruyama, H., Moulder, G., Maruyama, I., Barstead, R., & Rand, J. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.10.3441 · Cited by 93 · see citing works
Deguchi‐Tawarada, M., Inoue, E., Takao‐Rikitsu, E., Inoue, M., Ohtsuka, T., & Takai, Y. (2004) · Genes to Cells · doi:10.1111/j.1356-9597.2004.00697.x · Cited by 89 · see citing works
Improved detection of small deletions in complex pools of DNA.
Edgley, M., D'Souza, A., Moulder, G., McKay, S., Shen, B., Gilchrist, E., Moerman, D., & Barstead, R. (2002) · Nucleic Acids Research · doi:10.1093/nar/gnf051 · Cited by 86 · see citing works
Presynaptic terminal differentiation: transport and assembly
Zhen, M., & Jin, Y. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.05.013 · Cited by 66 · see citing works
Nakata, T., Yokota, T., Emi, M., & Minami, S. (2002) · Genes Chromosomes and Cancer · doi:10.1002/gcc.10095 · Cited by 27 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Südhof, T. C. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.012 · Cited by 1,062 · see citing works
Wagh, D. A., Rasse, T. M., Asan, E., Hofbauer, A., Schwenkert, I., Dürrbeck, H., Buchner, S., Dabauvalle, M.-C., Schmidt, M., Qin, G., et al. (2006) · Neuron · doi:10.1016/j.neuron.2006.02.008 · Cited by 908 · see citing works
Molecular organization of the presynaptic active zone
Schoch, S., & Gundelfinger, E. D. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0244-y · Cited by 334 · see citing works
Analysis of synaptic transmission in Caenorhabditis elegans using an aldicarb-sensitivity assay
Mahoney, T. R., Luo, S., & Nonet, M. L. (2006) · Nature Protocols · doi:10.1038/nprot.2006.281 · Cited by 277 · see citing works
Self-citationThe Golgin Coiled-Coil Proteins of the Golgi ApparatusPreprint
Munro, S. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005256 · Cited by 226 · 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
Self-citationMolecular Mechanisms of Presynaptic Differentiation
Jin, Y., & Garner, C. C. (2008) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.23.090506.123417 · Cited by 184 · 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
RIM-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
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
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
Zhou, K.-M., Dong, Y., Ge, Q., Zhu, D. Y., Zhou, W., Lin, X., Liang, T., Wu, Z., & Xu, T. (2007) · Neuron · doi:10.1016/j.neuron.2007.09.015 · Cited by 88 · see citing works
Liprin-α/SYD-2 determines the size of dense projections in presynaptic active zones in C. elegans
Kittelmann, M., Hegermann, J., Goncharov, A., Taru, H., Ellisman, M. H., Richmond, J. E., Jin, Y., & Eimer, S. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201302022 · Cited by 78 · see citing works
CAST and ELKS proteins: structural and functional determinants of the presynaptic active zone
Hida, Y., & Ohtsuka, T. (2010) · The Journal of Biochemistry · doi:10.1093/jb/mvq065 · Cited by 78 · see citing works
Zhou, K., Stawicki, T. M., Goncharov, A., & Jin, Y. (2013) · eLife · doi:10.7554/elife.01180 · Cited by 79 · see citing works
RIM proteins and their role in synapse function
Mittelstaedt, T., Álvarez‐Barón, E., & Schoch, S. (2010) · Biological Chemistry · doi:10.1515/bc.2010.064 · Cited by 75 · see citing works
Dong, 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
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
Held, R. G., Liu, C., & Kaeser, P. S. (2016) · eLife · doi:10.7554/elife.14862 · Cited by 67 · see citing works
Kiyonaka, S., Nakajima, H., Takada, Y., Hida, Y., Yoshioka, T., Hagiwara, A., Kitajima, I., Mori, Y., & Ohtsuka, T. (2012) · The Journal of Biochemistry · doi:10.1093/jb/mvs054 · Cited by 65 · see citing works
Shen, Y., Ge, W., Li, Y., Hirano, A., Lee, H.-Y., Rohlmann, A., Missler, M., Tsien, R. W., Jan, L. Y., Fu, Y., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501364112 · Cited by 52 · see citing works
ELKS1 localizes the synaptic vesicle priming protein bMunc13-2 to a specific subset of active zones
Kawabe, H., Mitkovski, M., Kaeser, P. S., Hirrlinger, J., Opazo, F., Nestvogel, D., Kalla, S., Fejtova, A., Verrier, S. E., Bungers, S. R., et al. (2017) · Journal of Cell Biology · doi:10.1083/jcb.201606086 · Cited by 50 · see citing works
RSY-1 Is a Local Inhibitor of Presynaptic Assembly in C. elegans
Patel, M. R., & Shen, K. (2009) · Science · doi:10.1126/science.1169025 · Cited by 45 · see citing works
ELKS active zone proteins as multitasking scaffolds for secretion
Held, R. G., & Kaeser, P. S. (2018) · Open Biology · doi:10.1098/rsob.170258 · Cited by 43 · see citing works
Coupling the Structural and Functional Assembly of Synaptic Release Sites
Ghelani, T., & Sigrist, S. J. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00081 · Cited by 38 · see citing works
Arellano‐Carbajal, F., Briseño-Roa, L., Couto, A., Cheung, B. H. H., Labouesse, M., & de Bono, M. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001341 · Cited by 38 · see citing works
Inoue, E., Deguchi‐Tawarada, M., Takao‐Rikitsu, E., Inoue, M., Kitajima, I., Ohtsuka, T., & Takai, Y. (2006) · Genes to Cells · doi:10.1111/j.1365-2443.2006.00970.x · Cited by 38 · see citing works
Motor Neuron Synapse and Axon Defects in a C. elegans Alpha-Tubulin Mutant
Baran, R., Castelblanco, L., Tang, G., Шапиро, Я., Goncharov, A., & Jin, Y. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009655 · Cited by 35 · see citing works
UNC-41/Stonin Functions with AP2 to Recycle Synaptic Vesicles in Caenorhabditis elegans
Mullen, G. P., Grundahl, K. M., Gu, M., Watanabe, S., Hobson, R. J., Crowell, J. A., McManus, J. R., Mathews, E., Jørgensen, E. M., & Rand, J. B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040095 · Cited by 32 · see citing works
Böhme, M. A., Grasskamp, A. T., & Walter, A. M. (2018) · FEBS Letters · doi:10.1002/1873-3468.13188 · Cited by 32 · see citing works
Presynaptic development is controlled by the core active zone proteins CAST/ELKS
Radulović, T., Dong, W., Goral, R. O., Thomas, C. I., Veeraraghavan, P., Montesinos, M. S., Guerrero‐Given, D., Goff, K. M., Lübbert, M., Kamasawa, N., et al. (2020) · The Journal of Physiology · doi:10.1113/jp279736 · Cited by 29 · see citing works
Neurotransmitter release mechanisms studied in Caenorhabditis elegans
Barclay, J. W., Morgan, A., & Burgoyne, R. D. (2012) · Cell Calcium · doi:10.1016/j.ceca.2012.03.005 · Cited by 29 · see citing works
Oh, 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
Torres, V. I., & Inestrosa, N. C. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0661-9 · Cited by 27 · see citing works
Synaptogenesis: unmasking molecular mechanisms using Caenorhabditis elegans
Mizumoto, K., Jin, Y., & Bessereau, J. (2023) · Genetics · doi:10.1093/genetics/iyac176 · Cited by 26 · see citing works
AIP limits neurotransmitter release by inhibiting calcium bursts from the ryanodine receptor
Chen, B., Liu, P., Hujber, E. J., Li, Y., Jørgensen, E. M., & Wang, Z.-W. (2017) · Nature Communications · doi:10.1038/s41467-017-01704-z · Cited by 26 · see citing works
Self-citationMechanisms controlling the trafficking, localization, and abundance of presynaptic Ca2+ channels
Cunningham, K. L., & Littleton, J. T. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1116729 · Cited by 25 · see citing works
Intrinsic and extrinsic mechanisms of synapse formation and specificity in C. elegans
Hendi, A., Kurashina, M., & Mizumoto, K. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03109-1 · Cited by 20 · see citing works
Liprin-α-Mediated Assemblies and Their Roles in Synapse Formation
Xie, X., Liang, M., Yu, C., & Wei, Z. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.653381 · Cited by 22 · see citing works
Dorfman, M. D., Gomes, J., O'Rourke, S., & Bowerman, B. A. (2009) · Genetics · doi:10.1534/genetics.109.104885 · Cited by 22 · see citing works
Crystal Structure of the RIM2 C2A-Domain at 1.4 Å Resolution,
Dai, H., Tomchick, D. R., García, J., Südhof, T. C., Machius, M., & Rizo, J. (2005) · Biochemistry · doi:10.1021/bi0513608 · Cited by 21 · see citing works
Presynaptic voltage-gated calcium channels in the auditory brainstem
Young, S. M., & Veeraraghavan, P. (2021) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2021.103609 · Cited by 19 · see citing works
CAST: Functional scaffold for the integrity of the presynaptic active zone
Ohtsuka, T. (2013) · Neuroscience Research · doi:10.1016/j.neures.2013.03.003 · Cited by 19 · see citing works
Loucks, C. M., Park, K., Walker, D. S., McEwan, A. H., Timbers, T. A., Ardiel, E. L., Grundy, L. J., Li, C., Johnson, J.-L., Kennedy, J., et al. (2019) · eLife · doi:10.7554/elife.37271 · Cited by 18 · see citing works
Nuclear pre-mRNA 3′-end processing regulates synapse and axon development in C. elegans
Epps, H. V., Dai, Y., Qi, Y. B., Goncharov, A., & Jin, Y. (2010) · Development · doi:10.1242/dev.049692 · Cited by 18 · see citing works
CAST: Its molecular structure and phosphorylation-dependent regulation of presynaptic plasticity
Hamada, S., & Ohtsuka, T. (2017) · Neuroscience Research · doi:10.1016/j.neures.2017.12.005 · Cited by 15 · see citing works
FIONA on Caenorhabditis elegans
Kural, C., Nonet, M. L., & Selvin, P. R. (2009) · Biochemistry · doi:10.1021/bi8023477 · Cited by 14 · see citing works
Self-citationOlesnicky, E. C., Antonacci, S., Popitsch, N. P., Lybecker, M. C., Titus, M. B., Valadez, R., Derkach, P. G., Marean, A., Miller, K., Mathai, S. K., et al. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.09.022 · Cited by 11 · see citing works
Macromolecular complexes at active zones: integrated nano-machineries for neurotransmitter release
Chua, J. J. E. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1657-5 · Cited by 9 · see citing works
Morrison, L. M., Edwards, S. L., Manning, L., Stec, N., Richmond, J. E., & Miller, K. G. (2018) · Genetics · doi:10.1534/genetics.118.300847 · Cited by 8 · see citing works
The Yin and Yang of Synaptic Active Zone Assembly
Sigrist, S. J. (2009) · Science Signaling · doi:10.1126/scisignal.270pe32 · Cited by 5 · see citing works
Kurashina, M., Snow, A. W., & Mizumoto, K. (2024) · Genetics · doi:10.1093/genetics/iyae214 · Cited by 4 · see citing works
Voltage-Gated Calcium Channels (VGCCs) and Synaptic Transmission
Saghian, R., & Wang, L. (2022) · Springer eBooks · doi:10.1007/978-3-031-08881-0_12 · Cited by 3 · see citing works
Presynaptic Cytomatrix Proteins
Jin, Y., & Zhai, R. G. (2023) · Advances in neurobiology · doi:10.1007/978-3-031-34229-5_2 · Cited by 3 · see citing works
Ndm, a coiled-coil domain protein that suppresses macropinocytosis and has effects on cell migration
Kelsey, J. S., Fastman, N. M., Noratel, E. F., & Blumberg, D. D. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-05-0392 · Cited by 3 · see citing works
Characterization of synaptic protein complexes in Drosophila melanogaster
Schmidt, M. (2006) · doi:10.53846/goediss-3597 · Cited by 2 · see citing works
Blobby is a synaptic active zone assembly protein required for memory in Drosophila
Lützkendorf, J., Matkovic, T., Liu, S., Götz, T., Gao, L., Turrel, O., Maglione, M., Grieger, M., Putignano, S., Ramesh, N., et al. (2025) · Nature Communications · doi:10.1038/s41467-024-55382-9 · Cited by 1 · see citing works
Network of Protein-Protein Interactions at the Presynaptic Active Zone
Ohtsuka, T. (2014) · Springer eBooks · doi:10.1007/978-4-431-55166-9_3 · Cited by 1 · see citing works
Structure and Function of Vertebrate and Invertebrate Active Zones
Garner, C. C., & Shen, K. (2008) · Springer eBooks · doi:10.1007/978-0-387-77232-5_3 · Cited by 1 · see citing works
Liprins, ELKS, and RIM-BP Proteins
Schoch, S., Mittelstaedt, T., & Zürner, M. (2009) · Elsevier eBooks · doi:10.1016/b978-008045046-9.01369-3
Early Active Zone Assembly in Drosophila
Owald, D. (2010) · doi:10.53846/goediss-3258
Characterization of synaptic protein complexes in Drosophila
Schmidt, M., Wichmann, C., Mertel, S., Sigrist, C., Schmidt, A., & Schwarz, T. (2013)
Presynaptic Terminal Differentiation
Zhen, M. (2007) · Elsevier eBooks · doi:10.1016/b978-012369437-9/50008-6
A transcriptional program remodels GABAergic synapses in C. elegans
Petersen, S. C. (2011)
Presynaptic Mechanisms for Cargo Recruitment
Nyitrai, H. (2019) · Digital Access to Scholarship at Harvard (DASH) (Harvard University)
Roles of the ELKS/CAST Family and SAD Kinase in Neurotransmitter Release
Ohtsuka, T., & Takai, Y. (2008) · Humana Press eBooks · doi:10.1007/978-1-59745-481-0_8
Liprins, ELKS, and RIM-BP Proteins
Schoch, S., Müller, J. A., Schönhense, E. M., & Betzin, J. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.04655-9
Wong, M. Y., & Kaeser, P. S. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.04486-x
Identification and characterization of a synaptic active zone assembly proteinPreprint
Lützkendorf, J., Matkovic, T., Götz, T., Liu, S., Ghelani, T., Maglione, M., Grieger, M., Putignano, S., Gao, L., Gimber, N., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.08.588536
A modular system to label endogenous presynaptic proteins using split fluorophores in C. elegansPreprint
Kurashina, M., Snow, A. W., & Mizumoto, K. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.29.605690
CAST/ELKS–endophilin-A interaction ensures synaptic vesicle pool size
Mori, Y., Sakamoto, H., Kim, Y., Hamada, S., Kaku, F., Hida, Y., Hirose, K., & Ohtsuka, T. (2026) · The Journal of Cell Biology · doi:10.1083/jcb.202508077
- Authors
- Deken, S. L., Vincent, R., Hadwiger, G., Liu, Q., Wang, Z.-W., & Nonet, M. L.
- Affiliations
- Washington University in St. Louis (US)
- UConn Health (US)
- Corresponding author
- Nonet, Michael L.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2005-06-22
- Volume
- 25
- Issue
- 25
- Pages
- 5975-5983
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6724794
- OpenAlex
- W2029712139
- Cited by
- 72
- References
- 48
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 3 · 2023: 4 · 2022: 1 · 2021: 3 · 2020: 2 · 2019: 3 · 2018: 6 · 2017: 4 · 2016: 1 · 2015: 3 · 2014: 4 · 2013: 4 · 2012: 6
- FWCI
- 1.45
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (1f32ns047000-01)
- National Institute of Neurological Disorders and Stroke (5 F32 NS047000, R01NS033535)
- 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 › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- RIM, elk, active zone proteins, protein localization, PDZ domain, synaptic transmission, neurotransmitter release, Caenorhabditis elegans, unc-10, protein-protein interaction, release sites
- MeSH terms
- Animals, Carrier Proteins, Cloning, Molecular, Electrophysiology, Synaptic Transmission, Synapses, Caenorhabditis elegans, Caenorhabditis elegans Proteins, Intracellular Signaling Peptides and Proteins
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