Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming
Open accessAbstract
Synaptic vesicles must be primed to fusion competence before they can fuse with the plasma membrane in response to increased intracellular Ca 2+ levels. The presynaptic active zone protein Munc13-1 is essential for priming of glutamatergic synaptic vesicles in hippocampal neurons. However, a small subpopulation of synapses in any given glutamatergic nerve cell as well as all γ-aminobutyratergic (GABAergic) synapses are largely independent of Munc13-1. We show here that Munc13-2, the only Munc13 isoform coexpressed with Munc13-1 in hippocampus, is responsible for vesicle priming in Munc13-1 independent hippocampal synapses. Neurons lacking both Munc13-1 and Munc13-2 show neither evoked nor spontaneous release events, yet form normal numbers of synapses with typical ultrastructural features. Thus, the two Munc13 isoforms are completely redundant in GABAergic cells whereas glutamatergic neurons form two types of synapses, one of which is solely Munc13-1 dependent and lacks Munc13-2 whereas the other type employs Munc13-2 as priming factor. We conclude that Munc13-mediated vesicle priming is not a transmitter specific phenomenon but rather a general and essential feature of multiple fast neurotransmitter systems, and that synaptogenesis during development is not dependent on synaptic secretory activity.
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?
Munc13-1/2 are putative markers of primed vesicles.
“and Munc13-1/2, putative markers of primed vesicles [14,42–45,60,61].”
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 [42]
The Discussion reports that removing both Munc13-1 and Munc13-2 eliminates readily releasable vesicles and arrests vesicle priming in mature hippocampal neurons. This supports their role as priming factors, but the paper does not establish that either protein serves as a marker identifying primed vesicles. (LLM, conf=0.82)
Experimental — accuracy not yet measuredbMunc13-2 is the second-most abundant isoform expressed at mossy fiber bouton synapses.
“After Munc13-1, the second-most abundant isoform expressed at MFB synapses is bMunc13-2 [40,42,77].”
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 [42]
The Discussion (page unavailable) says glutamatergic hippocampal synapses can be differentially equipped with Munc13-1 and Munc13-2. It does not identify the bMunc13-2 splice variant at mossy fiber bouton synapses or rank its abundance there; searches for those terms found no such passage. (LLM, conf=0.82)
Experimental — accuracy not yet measuredForskolin slightly reduces the distance between CaV2.1 Ca2+ channels and Munc13-1.
“Furthermore, we discovered that forskolin slightly reduced the distance between CaV2.1 (P/Q-type) Ca2+ channels and Munc13-1, an essential vesicle priming protein and putative marker of primed vesicles [14,40–45].”
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 [42]
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
Target-cell-specific facilitation and depression in neocortical circuits
Reyes, A., Lujan, R., Rozov, A., Burnashev, N., Somogyi, P., & Sakmann, B. (1998) · Nature Neuroscience · doi:10.1038/1092 · Cited by 716 · 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
Self-citationTarget cell-specific modulation of transmitter release at terminals from a single axon
Scanziani, M., Gähwiler, B. H., & Charpak, S. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.12004 · Cited by 167 · see citing works
Differential expression of two novel Munc13 proteins in rat brain
AUGUSTIN, I., BETZ, A., HERRMANN, C., JO, T., & BROSE, N. (1999) · Biochemical Journal · doi:10.1042/bj3370363 · Cited by 151 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 21
- [1]Südhof T C. Nature (London) 1995;375:645–653. doi: 10.1038/375645a0. [[DOI](https://doi.org/10.1038/375645a0)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/7791897/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Nature%20(London)&author=T%20C%20S%C3%BCdhof&volume=375&publication_year=1995&pages=645-653&pmid=7791897&doi=10.1038/375645a0&)] · DOI
- [2]Zucker R S. Neuron. 1996;17:1049–1055. doi: 10.1016/s0896-6273(00)80238-x. [[DOI](https://doi.org/10.1016/s0896-6273(00)80238-x)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/8982154/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Neuron&author=R%20S%20Zucker&volume=17&publication_year=1996&pages=1049-1055&pmid=8982154&doi=10.1016/s0896-6273(00)80238-x&)] · DOI
- [3]Augustin I, Rosenmund C, Südhof T C, Brose N. Nature (London) 1999b;400:457–461. doi: 10.1038/22768. [[DOI](https://doi.org/10.1038/22768)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/10440375/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Nature%20(London)&author=I%20Augustin&author=C%20Rosenmund&author=T%20C%20S%C3%BCdhof&author=N%20Brose&volume=400&publication_year=1999b&pages=457-461&pmid=10440375&doi=10.1038/22768&)] · DOI · Paper page
- [4]Aravamudan B, Fergestad T, Davis W S, Rodesch C K, Broadie K. Nat Neurosci. 1999;2:965–971. doi: 10.1038/14764. [[DOI](https://doi.org/10.1038/14764)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/10526334/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Nat%20Neurosci&author=B%20Aravamudan&author=T%20Fergestad&author=W%20S%20Davis&author=C%20K%20Rodesch&author=K%20Broadie&volume=2&publication_year=1999&pages=965-971&pmid=10526334&doi=10.1038/14764&)] · DOI
- [5]Richmond J E, Davis W S, Jorgensen E M. Nat Neurosci. 1999;2:959–964. doi: 10.1038/14755. [[DOI](https://doi.org/10.1038/14755)] [[PMC free article](/articles/PMC2585767/)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/10526333/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Nat%20Neurosci&author=J%20E%20Richmond&author=W%20S%20Davis&author=E%20M%20Jorgensen&volume=2&publication_year=1999&pages=959-964&pmid=10526333&doi=10.1038/14755&)] · DOI
- [6]Rosenmund C, Sigler A, Augustin I, Reim K, Brose N, Rhee J-S. Neuron. 2002;33:411–424. doi: 10.1016/s0896-6273(02)00568-8. [[DOI](https://doi.org/10.1016/s0896-6273(02)00568-8)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/11832228/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Neuron&author=C%20Rosenmund&author=A%20Sigler&author=I%20Augustin&author=K%20Reim&author=N%20Brose&volume=33&publication_year=2002&pages=411-424&pmid=11832228&doi=10.1016/s0896-6273(02)00568-8&)] · DOI
- [7]Brose N, Hofmann K, Hata Y, Südhof T C. J Biol Chem. 1995;270:25273–25280. doi: 10.1074/jbc.270.42.25273. [[DOI](https://doi.org/10.1074/jbc.270.42.25273)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/7559667/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=J%20Biol%20Chem&author=N%20Brose&author=K%20Hofmann&author=Y%20Hata&author=T%20C%20S%C3%BCdhof&volume=270&publication_year=1995&pages=25273-25280&pmid=7559667&doi=10.1074/jbc.270.42.25273&)] · DOI · Paper page
- [8]Augustin I, Betz A, Herrmann C, Jo T, Brose N. Biochem J. 1999a;337:363–371. [[PMC free article](/articles/PMC1219986/)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/9895278/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Biochem%20J&author=I%20Augustin&author=A%20Betz&author=C%20Herrmann&author=T%20Jo&author=N%20Brose&volume=337&publication_year=1999a&pages=363-371&pmid=9895278&)]
- [10]Augustin I, Korte S, Rickmann M, Kretzschmar H A, Südhof T C, Herms J W, Brose N. J Neurosci. 2001;21:10–17. doi: 10.1523/JNEUROSCI.21-01-00010.2001. [[DOI](https://doi.org/10.1523/JNEUROSCI.21-01-00010.2001)] [[PMC free article](/articles/PMC6762458/)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/11150314/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=J%20Neurosci&author=I%20Augustin&author=S%20Korte&author=M%20Rickmann&author=H%20A%20Kretzschmar&author=T%20C%20S%C3%BCdhof&volume=21&publication_year=2001&pages=10-17&pmid=11150314&doi=10.1523/JNEUROSCI.21-01-00010.2001&)] · DOI
- [11]Reim K, Mansour M, Varoqueaux F, McMahon H T, Südhof T C, Brose N, Rosenmund C. Cell. 2001;104:71–81. doi: 10.1016/s0092-8674(01)00192-1. [[DOI](https://doi.org/10.1016/s0092-8674(01)00192-1)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/11163241/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Cell&author=K%20Reim&author=M%20Mansour&author=F%20Varoqueaux&author=H%20T%20McMahon&author=T%20C%20S%C3%BCdhof&volume=104&publication_year=2001&pages=71-81&pmid=11163241&doi=10.1016/s0092-8674(01)00192-1&)] · DOI
- [12]Thomas K R, Capecchi M R. Cell. 1987;51:503–512. doi: 10.1016/0092-8674(87)90646-5. [[DOI](https://doi.org/10.1016/0092-8674(87)90646-5)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/2822260/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Cell&author=K%20R%20Thomas&author=M%20R%20Capecchi&volume=51&publication_year=1987&pages=503-512&pmid=2822260&doi=10.1016/0092-8674(87)90646-5&)] · DOI · Paper page
- [13]Bekkers J M, Stevens C F. Proc Natl Acad Sci USA. 1991;88:7834–7838. doi: 10.1073/pnas.88.17.7834. [[DOI](https://doi.org/10.1073/pnas.88.17.7834)] [[PMC free article](/articles/PMC52398/)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/1679238/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Proc%20Natl%20Acad%20Sci%20USA&author=J%20M%20Bekkers&author=C%20F%20Stevens&volume=88&publication_year=1991&pages=7834-7838&pmid=1679238&doi=10.1073/pnas.88.17.7834&)] · DOI
- [14]Rosenmund C, Feltz A, Westbrook G L. J Neurosci. 1995;15:2788–2795. doi: 10.1523/JNEUROSCI.15-04-02788.1995. [[DOI](https://doi.org/10.1523/JNEUROSCI.15-04-02788.1995)] [[PMC free article](/articles/PMC6577776/)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/7536820/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=J%20Neurosci&author=C%20Rosenmund&author=A%20Feltz&author=G%20L%20Westbrook&volume=15&publication_year=1995&pages=2788-2795&pmid=7536820&doi=10.1523/JNEUROSCI.15-04-02788.1995&)] · DOI
- [15]Rosenmund C, Stevens C F. Neuron. 1996;16:1197–1207. doi: 10.1016/s0896-6273(00)80146-4. [[DOI](https://doi.org/10.1016/s0896-6273(00)80146-4)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/8663996/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Neuron&author=C%20Rosenmund&author=C%20F%20Stevens&volume=16&publication_year=1996&pages=1197-1207&pmid=8663996&doi=10.1016/s0896-6273(00)80146-4&)] · DOI
- [16]Ryan T A, Smith S J, Reuter H. Proc Natl Acad Sci USA. 1996;93:5567–5571. doi: 10.1073/pnas.93.11.5567. [[DOI](https://doi.org/10.1073/pnas.93.11.5567)] [[PMC free article](/articles/PMC39287/)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/8643616/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Proc%20Natl%20Acad%20Sci%20USA&author=T%20A%20Ryan&author=S%20J%20Smith&author=H%20Reuter&volume=93&publication_year=1996&pages=5567-5571&pmid=8643616&doi=10.1073/pnas.93.11.5567&)] · DOI
- [17]Murthy V N, Sejnowski T J, Stevens C F. Neuron. 1997;18:599–612. doi: 10.1016/s0896-6273(00)80301-3. [[DOI](https://doi.org/10.1016/s0896-6273(00)80301-3)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/9136769/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Neuron&author=V%20N%20Murthy&author=T%20J%20Sejnowski&author=C%20F%20Stevens&volume=18&publication_year=1997&pages=599-612&pmid=9136769&doi=10.1016/s0896-6273(00)80301-3&)] · DOI
- [18]Cochilla A J, Angleson J K, Betz W J. Annu Rev Neurosci. 1999;22:1–10. doi: 10.1146/annurev.neuro.22.1.1. [[DOI](https://doi.org/10.1146/annurev.neuro.22.1.1)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/10202529/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Annu%20Rev%20Neurosci&author=A%20J%20Cochilla&author=J%20K%20Angleson&author=W%20J%20Betz&volume=22&publication_year=1999&pages=1-10&pmid=10202529&doi=10.1146/annurev.neuro.22.1.1&)] · DOI
- [19]Ashery U, Varoqueaux F, Voets T, Betz A, Thakur P, Koch H, Neher E, Brose N, Rettig J. EMBO J. 2000;19:3586–3595. doi: 10.1093/emboj/19.14.3586. [[DOI](https://doi.org/10.1093/emboj/19.14.3586)] [[PMC free article](/articles/PMC313963/)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/10899113/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=EMBO%20J&author=U%20Ashery&author=F%20Varoqueaux&author=T%20Voets&author=A%20Betz&author=P%20Thakur&volume=19&publication_year=2000&pages=3586-3595&pmid=10899113&doi=10.1093/emboj/19.14.3586&)] · DOI
- [20]Betz A, Ashery U, Rickmann M, Augustin I, Neher E, Südhof T C, Rettig J, Brose N. Neuron. 1998;21:123–136. doi: 10.1016/s0896-6273(00)80520-6. [[DOI](https://doi.org/10.1016/s0896-6273(00)80520-6)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/9697857/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Neuron&author=A%20Betz&author=U%20Ashery&author=M%20Rickmann&author=I%20Augustin&author=E%20Neher&volume=21&publication_year=1998&pages=123-136&pmid=9697857&doi=10.1016/s0896-6273(00)80520-6&)] · DOI · Paper page
- [22]Thomson A M. J Physiol. 1997;502:131–147. doi: 10.1111/j.1469-7793.1997.131bl.x. [[DOI](https://doi.org/10.1111/j.1469-7793.1997.131bl.x)] [[PMC free article](/articles/PMC1159577/)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/9234202/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=J%20Physiol&author=A%20M%20Thomson&volume=502&publication_year=1997&pages=131-147&pmid=9234202&doi=10.1111/j.1469-7793.1997.131bl.x&)] · DOI
- [24]Verhage M, Maia A S, Plomp J J, Brussaard A B, Heeroma J H, Vermeer H, Toonen R F, Hammer R E, van den Berg T K, Missler M, Geuze H J, Südhof T C. Science. 2000;287:864–869. doi: 10.1126/science.287.5454.864. [[DOI](https://doi.org/10.1126/science.287.5454.864)] [[PubMed](https://pubmed.ncbi.nlm.nih.gov/10657302/)] [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Science&author=M%20Verhage&author=A%20S%20Maia&author=J%20J%20Plomp&author=A%20B%20Brussaard&author=J%20H%20Heeroma&volume=287&publication_year=2000&pages=864-869&pmid=10657302&doi=10.1126/science.287.5454.864&)] · DOI
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
Activity-driven local ATP synthesis is required for synaptic function
Rangaraju, V., Calloway, N., & Ryan, T. A. (2014) · Cell · doi:10.1016/j.cell.2013.12.042 · Cited by 836 · see citing works
Structure, Function, and Pharmacology of Glutamate Receptor Ion Channels
Hansen, K. B., Wollmuth, L. P., Bowie, D., Furukawa, H., Menniti, F. S., Sobolevsky, A. I., Swanson, G. T., Swanger, S. A., Greger, I. H., Nakagawa, T., et al. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000131 · Cited by 686 · see citing works
Genetic variability in the regulation of gene expression in ten regions of the human brain
UK Brain Expression Consortium, Ramasamy, A., North American Brain Expression Consortium, Trabzuni, D., Guelfi, S., Varghese, V., Smith, C., Walker, R., De, T., Coin, L., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3801 · Cited by 644 · see citing works
Ultrafast endocytosis at mouse hippocampal synapses
Watanabe, S., Rost, B. R., Camacho-Pérez, M., Davis, M. W., Söhl-Kielczynski, B., Rosenmund, C., & Jorgensen, E. M. (2013) · Nature · doi:10.1038/nature12809 · Cited by 607 · see citing works
Self-citationThe Morphological and Molecular Nature of Synaptic Vesicle Priming at Presynaptic Active Zones
Imig, C., Min, S.-W., Krinner, S., Arancillo, M., Rosenmund, C., Südhof, T. C., Rhee, J., Brose, N., & Cooper, B. H. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.009 · Cited by 389 · see citing works
Self-citationMunc13 mediates the transition from the closed syntaxin–Munc18 complex to the SNARE complex
Ma, C., Li, W., Xu, Y., & Rizo, J. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2047 · Cited by 363 · see citing works
The cell biology of synapse formation
Südhof, T. C. (2021) · Journal of Cell Biology · doi:10.1083/jcb.202103052 · Cited by 358 · see citing works
Defining the role of GABA in cortical development
Wang, D. D., & Kriegstein, A. R. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.167635 · Cited by 336 · 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
Munc13 C2B domain is an activity-dependent Ca2+ regulator of synaptic exocytosis
Shin, O.-H., Lu, J., Rhee, J.-S., Tomchick, D. R., Pang, Z. P., Wojcik, S. M., Camacho-Perez, M., Brose, N., Machius, M., Rizo, J., et al. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1758 · Cited by 243 · see citing works
Self-citationMHCI negatively regulates synapse density during the establishment of cortical connections
Glynn, M. W., Elmer, B. M., Garay, P. A., Liu, X.-B., Needleman, L. A., El-Sabeawy, F., & McAllister, A. K. (2011) · Nature Neuroscience · doi:10.1038/nn.2764 · Cited by 198 · see citing works
Mechanism of neurotransmitter release coming into focus
Rizo, J. (2018) · Protein Science · doi:10.1002/pro.3445 · Cited by 210 · see citing works
Lipstein, N., Sakaba, T., Cooper, B. H., Lin, K.-H., Strenzke, N., Ashery, U., Rhee, J.-S., Taschenberger, H., Neher, E., & Brose, N. (2013) · Neuron · doi:10.1016/j.neuron.2013.05.011 · Cited by 165 · see citing works
Self-citationFusion 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
SNAREopathies: Diversity in Mechanisms and Symptoms
Verhage, M., & Sørensen, J. B. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.036 · Cited by 121 · 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
An active vesicle priming machinery suppresses axon regeneration upon adult CNS injury
Hilton, B. J., Husch, A., Schaffran, B., Lin, T.-C., Burnside, E. R., Dupraz, S., Schelski, M., Kim, J., Müller, J. A., Schoch, S., et al. (2022) · Neuron · doi:10.1016/j.neuron.2021.10.007 · Cited by 116 · see citing works
Self-citationChen, Z., Cooper, B., Kalla, S., Varoqueaux, F., & Young, S. M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.5128-12.2013 · Cited by 102 · see citing works
Self-citationApproaches and Limitations in the Investigation of Synaptic Transmission and Plasticity
Glasgow, S. D., McPhedrain, R., Madranges, J. F., Kennedy, T. E., & Ruthazer, E. S. (2019) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2019.00020 · Cited by 100 · see citing works
Deletion of α‐neurexins does not cause a major impairment of axonal pathfinding or synapse formation
Dudanova, I., Tabuchi, K., Rohlmann, A., Südhof, T. C., & Missler, M. (2007) · Journal of Comparative Neurology · doi:10.1002/cne.21305 · Cited by 98 · see citing works
Hagiwara, A., Fukazawa, Y., Deguchi‐Tawarada, M., Ohtsuka, T., & Shigemoto, R. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20633 · Cited by 90 · see citing works
Electrical Stimulation and Motor Recovery
Young, W. (2015) · Cell Transplantation · doi:10.3727/096368915x686904 · Cited by 76 · see citing works
Molecular and functional architecture of striatal dopamine release sites
Banerjee, A., Imig, C., Balakrishnan, K., Kershberg, L., Lipstein, N., Uronen, R.-L., Wang, J., Cai, X., Benseler, F., Rhee, J. S., et al. (2022) · Neuron · doi:10.1016/j.neuron.2021.10.028 · Cited by 58 · see citing works
Self-citationDisentangling the roles of RIM and Munc13 in synaptic vesicle localization and neurotransmission
Zarebidaki, F., Camacho, M., Brockmann, M. M., Trimbuch, T., Herman, M. A., & Rosenmund, C. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.1922-20.2020 · Cited by 37 · see citing works
Self-citationVariability in the Munc13-1 content of excitatory release sites.
Karlocai, M. R., Heredi, J., Benedek, T., Holderith, N., Lorincz, A., & Nusser, Z. (2021) · eLife · doi:10.7554/elife.67468 · Cited by 37 · 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-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
“To probe the Ca 2+ channel–sensor coupling topography, we targeted Ca V 2.1, the major type of presynaptic Ca 2+ channel in MFBs [58,59] and Munc13-1/2, putative markers of primed vesicles [14,42–45,60 ,61 ].”
InfluentialSelf-citation
- Authors
- Varoqueaux, F., Sigler, A., Rhee, J.-S., Brose, N., Enk, C., Reim, K., & Rosenmund, C.
- Affiliations
- Max-Planck-Institute for Experimental Medicine, Department of Molecular Neurobiology, D-37075 Göttingen, Germany; and Max-Planck-Institute for Biophysical Chemistry, Department of Membrane Biophysics, D-37077 Göttingen, Germany
- Max Planck Institute for Biophysical Chemistry (DE)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2002-06-17
- Volume
- 99
- Issue
- 13
- Pages
- 9037-9042
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC124419
- OpenAlex
- W2061342956
- Cited by
- 619
- References
- 4
- Citations by year
- 2026: 17 · 2025: 23 · 2024: 23 · 2023: 24 · 2022: 32 · 2021: 29 · 2020: 28 · 2019: 27 · 2018: 26 · 2017: 46 · 2016: 27 · 2015: 22 · 2014: 20 · 2013: 24 · 2012: 31
- FWCI
- 7.66
- 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)
- Max Planck Institute for Plasma Physics (submittedVersion)
- GRO (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- Munc13-1, synaptic vesicle priming, glutamatergic synapses, GABAergic synapses, synaptogenesis, spontaneous synaptic transmission, evoked neurotransmitter release, active zone, vesicle fusion, hippocampal neurons
- MeSH terms
- Animals, Endocytosis, Hippocampus, Microscopy, Electron, Molecular Sequence Data, Nerve Tissue Proteins, Synaptic Transmission, Synapses, Blotting, Western, Mice, Knockout, Intracellular Signaling Peptides and Proteins, 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
