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Protein Quantification at the Single Vesicle Level Reveals That a Subset of Synaptic Vesicle Proteins Are Trafficked with High Precision
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Protein sorting represents a potential point of regulation in neurotransmission because it dictates the protein composition of synaptic vesicles, the organelle that mediates transmitter release. Although the average number of most vesicle proteins has been estimated using bulk biochemical approaches (Takamori et al., 2006), no information exists on the intervesicle variability of protein number, and thus on the precision with which proteins are sorted to vesicles. To address this, we adapted a single molecule quantification approach (Mutch et al., 2007) and used it to quantify both the average number and variance of seven integral membrane proteins in brain synaptic vesicles. We report that four vesicle proteins, SV2, the proton ATPase, Vglut1, and synaptotagmin 1, showed little intervesicle variation in number, indicating they are sorted to vesicles with high precision. In contrast, the apparent number of VAMP2/synaptobrevin 2, synaptophysin, and synaptogyrin demonstrated significant intervesicle variability. These findings place constraints on models of protein function at the synapse and raise the possibility that changes in vesicle protein expression affect vesicle composition and functioning.
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“SV2A is a promising biomarker of synaptic density as it is ubiquitously and, for the most part, homogeneously present in synaptic vesicles [47] with low variation in copy number per vesicle [66].”
From Challenges and rewards of in vivo synaptic density imaging, and its application to the study of depression (2025) · cites this paper as [66]
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LIMPERT, E., STAHEL, W. A., & ABBT, M. (2001) · BioScience · doi:10.1641/0006-3568(2001)051[0341:lndats]2.0.co;2 · Cited by 2,621
Molecular anatomy of a trafficking organelle
Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., et al. (2006) · Cell · doi:10.1016/j.cell.2006.10.030 · Cited by 2,373
STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis
Willig, K. I., Rizzoli, S. O., Westphal, V., Jahn, R., & Hell, S. W. (2006) · Nature · doi:10.1038/nature04592 · Cited by 1,236
Mirnics, K., Middleton, F. A., Marquez, A., Lewis, D. A., & Levitt, P. (2000) · Neuron · doi:10.1016/s0896-6273(00)00085-4 · Cited by 882
TURNOVER OF TRANSMITTER AND SYNAPTIC VESICLES AT THE FROG NEUROMUSCULAR JUNCTION
Ceccarelli, B., Hurlbut, W. P., & Mauro, A. (1973) · The Journal of Cell Biology · doi:10.1083/jcb.57.2.499 · Cited by 837
Buckley, K. M., & Kelly, R. B. (1985) · The Journal of Cell Biology · doi:10.1083/jcb.100.4.1284 · Cited by 713
Wojcik, S. M., Rhee, J. S., Herzog, É., Sigler, A., Jahn, R., Takamori, S., Brose, N., & Rosenmund, C. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401764101 · Cited by 510
Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles
Thiele, C., Hannah, M. J., Fahrenholz, F., & Huttner, W. B. (2000) · Nature Cell Biology · doi:10.1038/71366 · Cited by 498
Disposable Microfluidic Devices: Fabrication, Function, and Application
Fiorini, G. S., & Chiu, D. T. (2005) · BioTechniques · doi:10.2144/05383rv02 · Cited by 484
Self-citationOrigin of variability in quantal size in cultured hippocampal neurons and hippocampal slices.
Bekkers, J. M., Richerson, G. B., & Stevens, C. F. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.14.5359 · Cited by 452
Research works printed but not linked: 1
- Press WH (2001) Numerical recipes in Fortran 77: the art of scientific computing, Ed 2 (with corrections) (Cambridge UP, Cambridge, UK; New York).
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Bodzęta, A., Kahms, M., & Klingauf, J. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.07.040 · Cited by 102
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Nowack, A., Malarkey, E. B., Yao, J., Bleckert, A., Hill, J., & Bajjalieh, S. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0029560 · Cited by 81
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Joensuu, M., Padmanabhan, P., Durisic, N., Bademosi, A. T., Cooper, E. J., Morrow, I. C., Harper, C. B., Jung, W., Parton, R. G., Goodhill, G. J., et al. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201604001 · Cited by 78
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Wittig, S., Ganzella, M., Barth, M., Kostmann, S., Riedel, D., Pérez-Lara, Á., Jahn, R., & Schmidt, C. (2021) · Nature Communications · doi:10.1038/s41467-021-21102-w · Cited by 60
Jiang, Y., Andronico, L., Jung, S., Chen, H., Fujimoto, B. S., Vojtech, L. N., & Chiu, D. T. (2021) · Angewandte Chemie International Edition · doi:10.1002/anie.202103282 · Cited by 53
Self-citationChen, L., Wu, L. J., Yu, J., Kuo, C.-T., Jian, T., Wu, I., Rong, Y., & Chiu, D. T. (2017) · Chemical Science · doi:10.1039/c7sc03448b · Cited by 53
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Jensen, B. K., Schuldi, M. H., McAvoy, K., Russell, K. A., Boehringer, A. V., Curran, B. M., Krishnamurthy, K., Wen, X., Westergard, T., Ma, L., et al. (2020) · EMBO Molecular Medicine · doi:10.15252/emmm.201910722 · Cited by 51
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Harlow, M. L., Szule, J. A., Xu, J., Jung, J. H., Marshall, R. M., & McMahan, U. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069410 · Cited by 46
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Smart, K., Liu, H., Matuskey, D., Chen, M.-K., Torres, K., Nabulsi, N., Labaree, D., Ropchan, J., Hillmer, A. T., Huang, Y., et al. (2021) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x20946198 · Cited by 42
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Wenzel, E. M., Morton, A., Ebert, K., Welzel, O., Kornhuber, J., Cousin, M. A., & Groemer, T. W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038188 · Cited by 42
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Keighron, J. D., Ewing, A. G., & Cans, A.-S. U. (2012) · The Analyst · doi:10.1039/c2an15901e · Cited by 40
Kljakic, O., Janíčková, H., Prado, V. F., & Prado, M. A. M. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14003 · Cited by 39
Morgan, J. R., Comstra, H. S., Cohen, M., & Faúndez, V. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016915 · Cited by 39
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López-Hernández, T., Takenaka, K.-I., Mori, Y., Kongpracha, P., Nagamori, S., Haucke, V., & Takamori, S. (2021) · eLife · doi:10.7554/elife.71198 · Cited by 38
Nguyen, A. T., Aerts, T., Dam, D. V., & Deyn, P. P. D. (2010) · Journal of Chromatography B · doi:10.1016/j.jchromb.2010.09.019 · Cited by 37
Guan, Z., Bykhovskaia, M., Jorquera, R. A., Sutton, R. B., Akbergenova, Y., & Littleton, J. T. (2017) · eLife · doi:10.7554/elife.28409 · Cited by 36
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Kroken, A. R., Karalewitz, A., Fu, Z., Kim, J. P., & Barbieri, J. T. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.254086 · Cited by 36
Li, H., Wu, C., Aramayo, R., Sachs, M. S., & Harlow, M. L. (2015) · Scientific Reports · doi:10.1038/srep14918 · Cited by 31
Gordon, S. L., Harper, C. B., Smillie, K. J., & Cousin, M. A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149457 · Cited by 34
Reductions in synaptic marker SV2A in early-course Schizophrenia
Yoon, J. H., Zhang, Z., Mormino, E. C., Davidzon, G., Minzenberg, M., Ballon, J. S., Kalinowski, A., Hardy, K. V., Naganawa, M., Carson, R. E., et al. (2023) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2023.02.026 · Cited by 36
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Siksou, L., Silm, K., Biesemann, C., Nehring, R. B., Wojcik, S. M., Triller, A., Mestikawy, S. E., Marty, S., & Herzog, É. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12199 · Cited by 37
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de Oliveira, G. P., Welsh, J. A., Pinckney, B., Palu, C. C., Lu, S., Zimmerman, A. J., Barbosa, R. H., Sahu, P., Noshin, M., Gummuluru, S., et al. (2023) · Journal of Extracellular Biology · doi:10.1002/jex2.107 · Cited by 31
Luo, F., Dittrich, M., Cho, S., Stiles, J. R., & Meriney, S. D. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00879.2014 · Cited by 33
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Mutch, S. A., Gadd, J. C., Fujimoto, B. S., Kensel-Hammes, P., Schiro, P. G., Bajjalieh, S., & Chiu, D. T. (2011) · Nature Protocols · doi:10.1038/nprot.2011.414 · Cited by 30
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Ramirez, D. M. O., & Kavalali, E. T. (2012) · Cellular Logistics · doi:10.4161/cl.20114 · Cited by 31
Bertoglio, D., Zajicek, F., Lombaerde, S. D., Miranda, A., Stroobants, S., Wang, Y., Dominguez, C., Munoz-Sanjuan, I., Bard, J., Liu, L., et al. (2022) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x221101648 · Cited by 29
Use Dependence of Presynaptic Tenacity
Fisher-Lavie, A., Zeidan, A., Stern, M., Garner, C. C., & Ziv, N. E. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3384-11.2011 · Cited by 29
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Metadata
- Authors
- Mutch, S. A., Kensel-Hammes, P., Gadd, J. C., Fujimoto, B. S., Allen, R. W., Schiro, P. G., Lorenz, R. M., Kuyper, C. L., Kuo, J. S., Bajjalieh, S. M., & Chiu, D. T.
- Affiliations
- University of Washington (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-01-26
- Volume
- 31
- Issue
- 4
- Pages
- 1461-1470
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3078718
- OpenAlex
- W2069765655
- Cited by
- 185
- References
- 39
- Citations by year
- 2026: 5 · 2025: 11 · 2024: 16 · 2023: 12 · 2022: 17 · 2021: 16 · 2020: 16 · 2019: 8 · 2018: 7 · 2017: 10 · 2016: 11 · 2015: 5 · 2014: 10 · 2013: 12 · 2012: 16
- FWCI
- 7.67
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Directorate for Biological Sciences
- University of California, Davis
- National Institute of Neurological Disorders and Stroke (U24NS050606, R01NS052637, NS052637)
- 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
- synaptic vesicle proteins, protein sorting, vesicle composition, SV2, VGLUT1, synaptotagmin-1, synaptophysin, H+-ATPase, neurotransmitter release, synaptic transmission
- MeSH terms
- Animals, Brain, Membrane Proteins, Synaptic Vesicles, Rats, Sprague-Dawley, Protein Transport, Rats, In Vitro Techniques
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