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Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography
Open accessAbstract
The presynaptic terminal contains a complex network of filaments whose precise organization and functions are not yet understood. The cryoelectron tomography experiments reported in this study indicate that these structures play a prominent role in synaptic vesicle release. Docked synaptic vesicles did not make membrane to membrane contact with the active zone but were instead linked to it by tethers of different length. Our observations are consistent with an exocytosis model in which vesicles are first anchored by long (>5 nm) tethers that give way to multiple short tethers once vesicles enter the readily releasable pool. The formation of short tethers was inhibited by tetanus toxin, indicating that it depends on soluble N-ethyl-maleimide sensitive fusion protein attachment protein receptor complex assembly. Vesicles were extensively interlinked via a set of connectors that underwent profound rearrangements upon synaptic stimulation and okadaic acid treatment, suggesting a role of these connectors in synaptic vesicle mobilization and neurotransmitter release.
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“In cryo-EM studies of unfixed and unstained synapse preparations, however, no dense projections are detectable. The only structures visible are the plasma membrane, synaptic vesicles, and sparse filaments that either connect vesicles to each others (“connectors,” average length ~10 nm) or tether vesicles to the presynaptic plasma membrane (“tethers”—5–20 nm; Landis et al., 1988; Fernández-Busnadie”
From The Presynaptic Active Zone (2012) · cites this paper as Fernández-Busnadiego et al., 2010
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“Besides these proteins, actin was suggested to be an active zone component, but high-resolution electron microscopy (EM) shows that actin filaments are excluded from the active zone and the vesicle cluster (Fernández-Busnadiego et al., 2010).”
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Citations
Cites
A simple method for organotypic cultures of nervous tissue
Stoppini, L., Buchs, P., & Muller, D. (1991) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(91)90128-m · Cited by 3,096
Südhof, T. C. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131412 · Cited by 2,491
Cryo-electron microscopy of vitrified specimens
Dubochet, J., Adrian, M., Chang, J.-J., Homo, J., Lepault, J., McDowall, A. W., & Schultz, P. (1988) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583500004297 · Cited by 2,397
Soille, P. (1999) · Springer eBooks · doi:10.1007/978-3-662-03939-7 · Cited by 1,981
Okadaic acid: a new probe for the study of cellular regulation
Cohen, P., Holmes, C. F. B., & Tsukitani, Y. (1990) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(90)90192-e · Cited by 1,373
Neurotoxins Affecting Neuroexocytosis
Schiavo, G., Matteoli, M., & Montecucco, C. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.2.717 · Cited by 1,266
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
Soille, P. (2004) · Springer eBooks · doi:10.1007/978-3-662-05088-0 · Cited by 1,065
Rizzoli, S. O., & Betz, W. J. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1583 · Cited by 975
Mechanisms of membrane fusion: disparate players and common principles
Martens, S., & McMahon, H. T. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2417 · Cited by 733
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Items 201–265 of 265
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Förster, F. G., Villa, E., Thomas, D. R., Korinek, A., & Baumeister, W. P. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-374920-8.00118-1 · Cited by 3
Self-citationGundersen, C. B. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18071582 · Cited by 3
Dynamic Compressed Sensing for Real-time Tomographic Reconstruction
Schwartz, J., Zheng, H., Hanwell, M. D., Jiang, Y., & Hovden, R. (2020) · Microscopy and Microanalysis · doi:10.1017/s1431927620021674 · Cited by 3
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Hoffmann, P. C., Giandomenico, S. L., Ganeva, I., Wozny, M. R., Sutcliffe, M. A., Kukulski, W., & Lancaster, M. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.23.216622 · Cited by 3
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Chakrabarti, R. (2018) · doi:10.53846/goediss-6685 · Cited by 3
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Peukes, J., Lovatt, C., Leistner, C., Boulanger, J., Morado, D. R., Fuller, M. J., Kukulski, W., Zhu, F., Komiyama, N. H., Briggs, J. A. G., et al. (2024) · eLife · doi:10.7554/elife.100335 · Cited by 5
Molecular and Morphological Correlates of Synaptic Vesicle Priming
Imig, C. (2014) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-4755 · Cited by 3
The molecular infrastructure of glutamatergic synapses in the mammalian forebrain
Peukes, J., Lovatt, C., Leistner, C., Boulanger, J., Morado, D. R., Fuller, M. J., Kukulski, W., Zhu, F., Komiyama, N. H., Briggs, J. A. G., et al. (2025) · eLife · doi:10.7554/elife.100335.3 · Cited by 2
Memory engram synapse 3D macromolecular architecture visualized by cryoCLEM-guided cryoET
Lovatt, C., O’Sullivan, T., Luis, C. O. S., Ryan, T. J., & Frank, R. A. W. (2025) · Structure · doi:10.1016/j.str.2025.10.014 · Cited by 3
Martínez-Sánchez, A., & Lučić, V. (2012) · Focus on structural biology · doi:10.1007/978-3-031-51171-4_11 · Cited by 2
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Marchand, S. J. L., & Dalva, M. B. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397266-8.00108-3 · Cited by 2
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Fukuda, Y., Leis, A. P., & Rigort, A. (2019) · doi:10.1002/9781118663233.ch19 · Cited by 2
Cryo-FIB workflow for imaging brain tissue via in situ cryo-electron microscopyPreprint
Ning, J., Glausier, J. R., Hsieh, C., Schmelzer, T., Buck, S. A., Franks, J. M., Hampton, C. M., Lewis, D. A., Marko, M., & Freyberg, Z. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.11.528064 · Cited by 2
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Galkov, M., Nemcova, P., Dietrich, D., & Schoch, S. (2026) · Advances in neurobiology · doi:10.1007/978-3-032-12594-1_4 · Cited by 1
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Do, T. T., Siegert, A., Domart, F., Hahn, F., Zeising, C., Muth, S., Pape, C., Kusch, K., Dresbach, T., Rizzoli, S. O., et al. (2026) · Structure · doi:10.1016/j.str.2026.02.017 · Cited by 2
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Mougios, N., Opazo, F., Rizzoli, S. O., & Reshetniak, S. (2023) · iScience · doi:10.1016/j.isci.2023.105971 · Cited by 1
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Nestvogel, D. (2017) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6444 · Cited by 1
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Peukes, J., Lovatt, C., Leistner, C., Boulanger, J., Morado, D. R., Fuller, M. J., Kukulski, W., Zhu, F., Komiyama, N. H., Briggs, J. A. G., et al. (2025) · eLife · doi:10.7554/elife.100335.2 · Cited by 1
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Baumeister, W. P. (2011) · NATO science for peace and security series. A, Chemistry and biology · doi:10.1007/978-94-007-2530-0_4
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Swulius, M. T. (2010) · Digital Commons-TMC (Texas Medical Center)
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Lučić, V., Baumeister, W. P., & Förster, F. G. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-374920-8.00211-3
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Short, B. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.1881iti3
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Marchand, S. J. L., & Dalva, M. B. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-823672-7.00005-3
Wong, M. Y., & Kaeser, P. S. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.04486-x · Cited by 1
Faculty Opinions recommendation of Variable priming of a docked synaptic vesicle.
Zucker, R. S. (2016) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.726131981.793525261
A role for synapsin 2a oligomerization in maintaining a reserve pool of synaptic vesicles
Zhang, M. (2022) · DR-NTU (Nanyang Technological University) · doi:10.32657/10356/159292
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Basta, T., Morgan, G., O'Toole, E. T., Rao, N. R., Savas, J. N., & Stowell, M. H. B. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2209-4_10
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Hintze, A. (2023) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-9828
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Mahfooz, K., Gotor, J. J. R., Pérez‐Otaño, I., & Wesseling, J. F. (2023) · eLife · doi:10.7554/elife.88212.1
Canales, M. R. (2023) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-9984
Kádková, A., Murach, J., Pedersen, M. Ø., Malsam, A., Malsam, J., Söllner, T. H., & Sørensen, J. B. (2023) · eLife · doi:10.7554/elife.88619.1
Kádková, A., Murach, J., Østergaard, M., Malsam, A., Malsam, J., Lolicato, F., Nickel, W., Söllner, T. H., & Sørensen, J. B. (2024) · doi:10.7554/elife.88619.2
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Gotor, J. J. R., Mahfooz, K., Pérez‐Otaño, I., & Wesseling, J. F. (2024) · eLife · doi:10.7554/elife.88212.2
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Rostami, I., Leuenberger, J., Ott, G., Nevian, T., & Zuber, B. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.11.687934
Self-citationDresbach, T. (2014) · Springer eBooks · doi:10.1007/978-4-431-55166-9_2
Vold, V. A., Yang, J., Østergaard, M., Lassen, A. S., Kádková, A., Kumar, A., Walter, A. M., Zhang, Y., & Sørensen, J. B. (2026) · Cell Reports · doi:10.1016/j.celrep.2025.116870
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McFadden, M. H. (2018) · theses.fr (ABES) · doi:10.70675/036294d9z53a4z495ez9221ze4fba667c298
Schorova, L. (2018) · theses.fr (ABES) · doi:10.70675/a30a505az5e81z4089za24azcf43d27e33ce
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Metadata
- Authors
- Fernández-Busnadiego, R., Zuber, B., Maurer, U. E., Cyrklaff, M., Baumeister, W., & Lučić, V.
- Affiliations
- Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, D-82152 Martinsried, Germany 1
- MRC Laboratory of Molecular Biology (GB)
- Max Planck Institute of Biochemistry (DE)
- Corresponding author
- Baumeister, Wolfgang
- Venue
- Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2010-01-11
- Volume
- 188
- Issue
- 1
- Pages
- 145-156
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC2812849
- OpenAlex
- W2132214171
- Cited by
- 267
- References
- 66
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 21 · 2023: 18 · 2022: 15 · 2021: 14 · 2020: 16 · 2019: 13 · 2018: 16 · 2017: 18 · 2016: 13 · 2015: 17 · 2014: 17 · 2013: 14 · 2012: 16
- FWCI
- 8.54
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Bern Open Repository and Information System (University of Bern) (submittedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- 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 › Structural Biology › Advanced Electron Microscopy Techniques and Applications
- Keywords
- synaptic vesicle release, docked vesicles, exocytosis, readily releasable pool, tetanus toxin, SNARE complex, okadaic acid, synaptic stimulation, neurotransmitter release, active zone, cryo-electron tomography
- MeSH terms
- Animals, Male, Synapses, Rats, Wistar, Tissue Culture Techniques, Rats, Electron Microscope Tomography
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